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Department of Zoology, Spatial Epidemiology and Ecology Group,
The Natural History Museum, Tinbergen Building, Department of Zoology,
London, UK University of Oxford, South Parks Road, Oxford, UK

Reader in Parasite Epidemiology, Immunology and Infection Section,
­Department of Infectious Disease Department of Biological Sciences,
Epidemiology, Faculty of Medicine Sir Alexander Fleming Building, ­Imperial
(St Mary’s campus), Imperial College, ­College of Science, Technology and
London, UK Medicine, London, UK

Wellcome Trust Research Fellow and Johns Hopkins Malaria Research Institute
Reader, London School of Hygiene and & Department of Epidemiology, Johns
Tropical Medicine, Faculty of Infectious Hopkins Bloomberg School of Public
and Tropical Diseases, London, UK Health, Baltimore, MD, USA

Department of Veterinary Science, The Head, WHO Collaborating Centre for
University of Melbourne, Parkville, the Molecular Epidemiology of Parasitic
­Victoria, Australia Infections, Principal Investigator, Envi­
ronmental Biotechnology CRC (EBCRC),
N. HALL School of Veterinary and Biomedical
School of Biological Sciences, Bio­ Sciences, Murdoch University, Murdoch,
sciences Building, University of Liver­ WA, Australia
pool, Liverpool, UK
R. C. OLIVEIRA Professor, Director, National Institute
Centro de Pesquisas Rene Rachou/ of Parasitic Diseases, Chinese Center
CPqRR - A FIOCRUZ em Minas Gerais, for Disease Control and Prevention,
Rene Rachou Research Center/CPqRR - ­Shanghai, People’s Republic of China
The Oswaldo Cruz Foundation in the
State of Minas Gerais-Brazil, Brazil
Advances in
Edited by

Department of Zoology,
The Natural History Museum,
Cromwell Road,
London, UK

Spatial Epidemiology and Ecology Group,
Tinbergen Building, Department of Zoology,
University of Oxford, South Parks Road,
Oxford, UK


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Kimberlee B. Beckmen
Alaska Department of Fish and Game, Division of Wildlife Conservation,
Fairbanks, AK, United States

Doug D. Colwell
Agriculture and Agri-food Canada, Lethbridge, Alberta, Canada

Joseph A. Cook
Museum of Southwestern Biology and Department of Biology, University
of New Mexico, Albuquerque, NM, USA

Bart Currie
Menzies School of Health Research, Casuarina, NT, Australia

Julie Ducrocq
Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta,

Brett T. Elkin
Environment and Natural Resources, Government of Northwest
­Territories, Yellowknife, Northwest Territories, Canada

Katja Fischer
Queensland Institute of Medical Research, Herston, Queensland, Australia

Kurt E. Galbreath
Department of Biology, Northern Michigan University, Marquette, MI, USA

Stephen E. Greiman
Department of Biology, University of North Dakota, Grand Forks, ND, USA

Ken Hashimoto
Chagas Disease Control Projects, Japan International Cooperation Agency,
Central America

Bryanne M. Hoar
Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta,

x        Contributors

Eric P. Hoberg
US National Parasite Collection, Animal Parasitic Diseases Laboratory,
Agricultural Research Service, USDA, Beltsville, MD, USA

Deborah Holt
Menzies School of Health Research, Casuarina, NT, Australia

David Kemp
Queensland Institute of Medical Research, Herston, Queensland, Australia

Susan J. Kutz
Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta,

Ian Maudlin
Division of Pathway Medicine and Centre for Infectious Diseases, School
of Biomedical Sciences, College of Medicine and Veterinary Medicine, The
University of Edinburgh, Edinburgh, UK

Lydden Polley
Western College of Veterinary Medicine, University of Saskatchewan,
­Saskatoon, Saskatchewan, Canada

Vasyl V. Tkach
Department of Biology, University of North Dakota, Grand Forks, ND, USA

Jefferson A. Vaughan
Department of Biology, University of North Dakota, Grand Forks, ND, USA

Guilherme G. Verocai
Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta,

Susan C. Welburn
Division of Pathway Medicine and Centre for Infectious Diseases, School
of Biomedical Sciences, College of Medicine and Veterinary Medicine, The
University of Edinburgh, Edinburgh, UK

Kota Yoshioka
Chagas Disease Control Project, Japan International Cooperation Agency,
Managua, Nicaragua
Northern Host–Parasite
Assemblages: History
and Biogeography on the
Borderlands of Episodic Climate
and Environmental Transition
Eric P. Hoberg*, Kurt E. Galbreath†, Joseph A. Cook‡,
Susan J. Kutz§, and Lydden Polley¶

Contents 1.1. Introduction 3

1.2. Northern Systems and Parasites – Setting the Stage 7
1.2.1. Developing knowledge of parasite diversity
in the North 9
1.2.2. Towards an integrated picture of parasite diversity 10
1.3. An Historical (Physical–Biological) Setting for the Arctic 12
1.3.1. Exploring the Beringian connection 15
1.4. Faunal Structure – Evidence for Northern Connections 17
1.4.1. Faunas associated with terrestrial Carnivora 17
1.4.2. Faunas associated with Lagomorpha 34
1.4.3. Faunas associated with Rodentia 39
1.4.4. Faunas associated with Artiodactyla 48
1.4.5. Human interfaces and occupation of the North 56

* US National Parasite Collection, Animal Parasitic Diseases Laboratory, Agricultural Research Service,
USDA, Beltsville, MD, USA,
†  Department of Biology, Northern Michigan University, Marquette, MI, USA,
‡ Museum of Southwestern Biology and Department of Biology, University of New Mexico,

Albuquerque, NM, USA,

§  Faculty of Veterinary Medicine, University of Calgary, Calgary, Alberta, Canada,
¶ Western College of Veterinary Medicine, University of Saskatchewan, Saskatoon, Saskatchewan,


Advances in Parasitology, Volume 79 © 2012 Elsevier Ltd.

ISSN 0091-679X, All rights reserved.

2     Eric P. Hoberg et al.

1.5. Biodiversity – History in a Complex Northern Fauna 60

1.5.1. General biogeographic patterns 63
1.5.2. Mechanisms of faunal expansion in space and time 66
1.5.3. An integrated model for diversification –
contributions from the North 69
1.5.4. Mosaic faunas – consequences of episodic
geographic expansion 70
1.5.5. Stories that parasites reveal 74
1.6. Tools for Biodiversity Discovery 76
1.7. Problems and Challenges to Be Resolved 79
Acknowledgements 81
References 81

Abstract Diversity among assemblages of mammalian hosts and parasites in

northern terrestrial ecosystems was structured by a deep history of
biotic and abiotic change that overlies a complex geographic arena.
Since the Pliocene, Holarctic ecosystems assembled in response to
shifting climates (glacial and interglacial stages). Cycles of episodic
dispersal/isolation and diversification defined northern diversity
on landscape to regional scales. Episodes of geographic expansion
and colonisation linked Eurasia and North America across Beringia
and drove macroevolutionary structure of host and parasite asso-
ciations. Asynchronous dispersal from centres of origin in Eurasia
into the Nearctic resulted in gradients in parasite diversity in the
carnivoran, lagomorph, rodent and artiodactyl assemblages we re-
viewed. Recurrent faunal interchange and isolation in conjunction
with episodes of host colonisation have produced a mosaic struc-
ture for parasite faunas and considerable cryptic diversity among
nematodes and cestodes. Mechanisms of invasion and geographic
colonisation leading to the establishment of complex faunal as-
semblages are equivalent in evolutionary and ecological time, as
demonstrated by various explorations of diversity in these high-
latitude systems. Our ability to determine historical responses
to episodic shifts in global climate may provide a framework for
predicting the cascading effects of contemporary environmental

Geography to a large extent determines climate and, in combination

with climate, provides the matrix within which ecosystems exist,
function and evolve.
David M. Hopkins, in Paleoecology of Beringia (1982).
The distributions of species that currently occur in the Arctic rep-
resent a snapshot of a dynamic and ongoing process driven by
historical ­climate changes….
Terry V. Callaghan et al. (2004c).
Northern Host–Parasite Assemblages     3

There are still some areas in the Arctic, especially in North America,
where it is possible to define natural parasite-host relationships, or
at least to gain an understanding of such relationships before the
arrival of Europeans.
Robert L. Rausch (1974).


The Earth’s northern circumpolar regions present landscapes of outstand-

ing beauty, incomparable fauna and flora and small, widely dispersed
human settlements. These are integrated biological systems, where peo-
ples of great resilience remain culturally close to the land and dependant
on an array of natural resources, while living with the extremes of short
summers and long cold winters (Rausch, 1951; Anisimov et al., 2007). The
North encompasses those regions extending from the borders of the Sub-
arctic (above 50°N) to beyond the Arctic Circle (north of 66°33′N) (Fig. 1.1).
The latter marks the approximate limit for the current northern treeline
and the circumpolar zone characterised seasonally by periods of constant
polar night or midnight sun. Treeless tundra habitats dominate the Arctic
where the average temperatures for the warmest month do not exceed
10°C; mean annual temperatures for the western subregions of the Arctic
range from −20 to +12°C with minimal precipitation varying from 5 to
150mm (Callaghan et al., 2004e). The Arctic transitions into more south-
erly Subarctic environments dominated primarily by taiga forests and a
more complex mosaic of habitats defined by latitude and altitude.
Northern ecosystems were formed by complex abiotic and biotic
mechanisms in a crucible driven by episodic climatological processes
and environmental perturbation extending across the late Pliocene and
Quaternary during the past 3–5 million years (Myr) (e.g. Hopkins et al.,
1982; Andersen and Borns, 1994 Dynesius and Jansson, 2000; Jansson and
Dynesius, 2002; Callaghan et al., 2004a,c; Hewitt, 2004a,b). Contemporary
patterns of faunal complexity reflect extinction events largely coincidental
with the thermal maximum that signalled the termination of continental
glaciation only 10 thousand years ago (Ka) (e.g. Barnosky et  al., 2004).
Consequently, northern biotas are typically characterised as relatively sim-
ple, low-diversity assemblages with short trophic linkages, few pathogens
and limited resilience or capacity for adaptation to environmental change
(e.g. Callaghan et al., 2004a) (Table 1.1). A gradient of declining diversity
with increasing latitude (from taiga forests to polar deserts) is also accom-
panied by a shift or increase in dominance for some species, which may
be manifested seasonally or annually (e.g. Callaghan et al., 2004b). High-
latitude biotas are now at their minimal extent relative to patterns of diver-
sity and geographic distribution that characterised faunas during the mid
to late Pleistocene (e.g. Guthrie, 1984; Callaghan et al., 2004a).
4     Eric P. Hoberg et al.

FIGURE 1.1  Boundaries and definitions for the Arctic and Subarctic regions according to
the Programme for the Conservation of Arctic Flora and Fauna (CAFF), shown in polar
projection. Boundaries can be defined by the isotherms, habitat, latitude or geopolitical
zones. Source map was developed by cartographer Philippe Rekacewicz (UNEP/GRID-
Arendal) and is made available by CAFF at
_of_the_arctic. (For color version of this figure, the reader is referred to the web version
of this book.)

At high latitudes, vulnerable systems of low diversity continue to

undergo significant and in some instances accelerating change due
largely to human activity, both local and distant. These perturbations
have the potential for broader impacts at a global scale (Callaghan
et  al., 2004a,d; Anisimov et  al., 2007; Lawler et  al., 2009; Post et  al.,
2009). Increasingly, substantial discussion has focused on the status and
future of northern ecosystems, but these assessments have been limited
Northern Host–Parasite Assemblages     5

TABLE 1.1  Defining characteristics for northern systems with respect to physical
and biological attributes (Irvine et al., 2000; Callaghan et al., 2004c,2004e; Hoberg
et al., 2008b)

Arctic Subarctic

Latitude > 66° 33′N > 50° N

Temperaturea < 10°C (mean summer) May exceed + 30°C
(maximum summer)
average low near −40°C
Small variation in extremes Great variation in
Precipitation Primarily snow (< 25cm) Snow and rain
(+ 40–45 cm)
Vegetation Shrub-tundra, tundra, polar Taiga, steppe, tundra
Latitudinal treeline, microhabi- Mosaics based on altitude
tat mosaics and latitude
Permafrost Present Present or absent
Diversity 75 species terrestrial mammals ± 250 species terrestrial
Vulnerability Habitat loss through climate Habitat perturbation
change through climate change
Responses (1) Populations at environmental extremes of distribution
in the Arctic (latitude, or altitude, mosaics within land-
scapes) respond to amelioration of physical conditions
such as limitations imposed by temperature through the
potential to expand based on both functional and numeri-
cal mechanisms?
(2) Populations at environmentally benign boundaries in the
Subarctic or with more southern distributions tend to be
constrained by competition with more responsive species,
and amelioration may drive shifts in distribution, devel-
opment of new ecotones, new patterns of sympatry and
a  Temperatures represent baselines from decades around 1980–1999.

to free-living organisms. Parasitism, pathogens and diseases have not

yet been an integral component of this discourse (Kutz et al., 2009a).
Parasites represent in excess of 40–50% of the organisms on Earth and
complex assemblages of macroparasites (helminths and arthropods) and
microparasites (viruses, bacteria and protozoans) shape ecosystems, food
webs, host demographics and behaviour (e.g. Marcogliese, 2005; Hudson
et  al., 2006; Dobson et  al., 2008). In some ecosystems, the biomass for
6     Eric P. Hoberg et al.

macroparasites exceeds that for apex predators such as birds and fishes,
suggesting a substantial role for otherwise obscure organisms at local to
regional scales (Kuris et al., 2008). Parasites can cause disease and mortal-
ity may influence the dynamics of wildlife populations and, in the worst-
case scenarios, contribute to extinction events.
Parasites are ubiquitous and diverse members of all biological commu-
nities including those at high latitudes. All animals in circumpolar regions
are susceptible to infection by characteristic assemblages of macroparasites
and microparasites. Parasites can have subtle to severe effects on individual
hosts or broader impacts on host populations that may cascade through
ecosystems. Parasitic diseases have dual significance: (1) influencing sus-
tainability for species and populations of diverse invertebrates, fishes, birds
and mammals and (2) secondarily affecting food security, quality and avail-
ability for people. Additionally, as zoonoses, some parasites can infect and
cause disease in people and are a primary issue for food safety and human
health (e.g. Kutz et al., 2009b; Jenkins et al., 2011). Sustainability, security
and safety of ‘country foods’ are of concern at northern latitudes where
people maintain a strong reliance on wildlife species. The potential signifi-
cance of zoonoses is magnified in the North by the intimate linkage between
wildlife and people. Subsistence food chains depend on the harvesting of
free-ranging mammals, birds and fish for food, fibre and other animal prod-
ucts. Understanding the role and influence of parasites in northern systems
emerges from explorations of history, biogeography and the intricate eco-
logical linkages among fishes, birds, mammals, domesticated species and
people in the context of broader global connections (e.g. Hoberg, 2010).
Despite the extreme environmental conditions in the North, the triad of
host, parasite and environment remains the key determinant of the profile
of parasitic infections and disease in people and animals. Parasites circulate
through pathways that link the host and environmental setting. Some para-
sites have direct transmission cycles that involve passage between definitive
hosts where the adult parasite develops and reproduces. Often, the infective
stages will occur free in the environment, sensitive to ambient temperature
and humidity, and are then acquired through ingestion of water or forage.
In contrast, indirect transmission is related to trophic connections between
predators (definitive) and prey (intermediate hosts where the parasite
develops) or may involve vectors, usually biting flies or other arthropods,
that disseminate the parasite between hosts. In the Arctic, the ambient envi-
ronmental setting (temperature, humidity, seasonality, geography, external
stressors), and life history traits and ecology of hosts (migration, hiberna-
tion, food habits, foraging behaviour, age and immunological status, etc.)
dramatically influence the survival, development, abundance and distribu-
tion of parasites and related disease in space and time (e.g. Kutz et al., 2004,
2005; Hoberg et al., 2008a,b; Kutz et al., 2009b; Laaksonen et al., 2010).
Northern Host–Parasite Assemblages     7



Parasites are important components of terrestrial, aquatic and marine

systems in the Arctic but seldom are included in general assessments of
biodiversity at high latitudes (Hoberg, 1996; Hoberg and Adams, 2000;
Hoberg et al., 2003; Kutz et al., 2009a). Climate change and associated eco-
logical perturbations are modifying the structure of terrestrial, aquatic and
marine systems across high latitudes of the north (e.g. ACIA, 2004; Rausch
et al., 2007; Hoberg et al., 2008a; Kutz et al., 2009b). Patterns of distribu-
tion, timing of migrations and seasonally defined windows that determine
the life histories for a diverse assemblage of vertebrates, invertebrates and
their parasites are under dynamic change (Callaghan et al., 2004d; Lawler
et  al., 2009). As we recognise and predict direct and indirect impacts to
terrestrial, aquatic and marine systems (e.g. Lawler et al., 2009; Post et al.,
2009), parasites and associated diseases should also be considered in the
‘equations’ for environmental change. Acclerating environmental pertur-
bation in northern ecosystems (particularly patterns of temperature and
humidity acting on habitat and distribution vertebrate and invertebrate
species) (ACIA, 2004) has a direct influence on the occurrence of parasites
and the potential for emergence of disease (Kutz et al., 2004, 2009a).
Cumulative (long-term) processes and extreme (short-term) events influ-
ence the occurrence of parasites and may mediate functional and numerical
responses that determine distribution (Hoberg et al., 2008b). Many northern
parasites are adapted to cold environments and short transmission win-
dows. Long-term processes such as incremental increases in global temper-
ature acting on regional and landscape scales can reduce generation times,
increase developmental rates and broaden seasonal windows for transmis-
sion (Hoberg et al., 2001; Kutz et al., 2005; Jenkins et al., 2006; Kutz et al.,
2012). In contrast, extreme weather events can result in the explosive emer-
gence of disease leading to mortality and morbidity at regional and local
scales (Ytrehus et  al., 2008; Laaksonen et  al., 2010). Significantly, extreme
events may emerge from patterns that are cumulative and established over
multiple years such as mortality events linked to the nematode Setaria in
reindeer that require successive seasons of atypically high temperatures as a
driver of population amplification (Laaksonen et al., 2010).
Amplification of parasite populations responding to either cumulative
or extreme events creates a background for cascading effects within ecosys-
tems that ultimately affects biodiversity for free-living and parasitic species
(Kutz, et al., 2005; Galaktionov et al., 2006; Kutz et al., 2009b). Concurrently,
northern range expansion for many vertebrate species will create new
opportunities for exposure of naive host populations to an array of patho-
gens (Brooks and Hoberg, 2006, 2007; Lawler et al., 2009; De Bruyn, 2010).
8     Eric P. Hoberg et al.

Interacting with overall habitat change and other biotic and abiotic factors,
disease can have an influence on the availability of food resources on which
northern communities are dependent. Consequently, parasites must be
explored (1) in the context of ecosystem function, stability and sustainabil-
ity; (2) as emerging pathogens that may directly influence subsistence food
webs and food security at high latitudes under a regime of environmen-
tal perturbation and (3) as potentially threatened components of northern
systems that may lack a capacity for adaptation to shifting environmental
conditions or may be eliminated through competition with new invaders
(e.g. Kutz et al., 2004, 2009b; Tryland et al., 2009; Laaksonen et al., 2010).
What had been a pursuit driven by curiosity has now gained currency
as a cornerstone in discussions about the fate of ecosystems and species
under a regime of accelerated climate change in northern systems. There
is an urgent need to document biodiversity for assemblages of proto-
zoan and helminth parasites at regional to local scales and particularly
those that are recognised and potential zoonoses (e.g. Rausch, 1972, 1974;
­Polley and Thompson, 2009). Concurrently, northern systems can serve
as models for change and cascading impacts on diversity as environmen-
tal perturbation expands (e.g. Hoberg, et al., 2008a,b; Kutz et al., 2009b).
Parasites have consequences for sustainability of tundra and high-latitude
ecosystems, wildlife populations, patterns of potential extinctions and
ultimately human occupation in the North where indigenous cultures
are dependent on subsistence food chains (Rausch, 1951; Callaghan et al.,
2004a; Brook et al., 2009) (Table 1.2).

TABLE 1.2  Why study parasites in the North?

General phenomena
• Ecological/historical indicators – the stories that parasites relate about the
biosphere in a continuum from evolutionary to ecological time (Brooks and
McLennan, 1993; Hoberg, 1997a)
• General models for transmission and disease explored in relatively low-diversity
systems (e.g. Irvine et al., 2000; Kutz et al., 2005; Laaksonen et al., 2010)
• Invasion biology in evolutionary and ecological time (Hoberg, 2010)
Environmental perturbation
• Unprecedented acceleration of environmental change in high-latitude
­systems relative to the Pleistocene (ACIA, 2004; Callaghan et al., 2004a)
• Necessity to understand host–parasite systems in a regime of accelerated
change (e.g. Hoberg et al., 2008a; Kutz et al., 2009b)
• Analogues for prediction about processes and impact (indirect and direct)
of environmental change (Hoberg, 1997a; Brooks and Hoberg, 2006)
• Ecosystem sustainability
• Food safety and security in high-latitude communities (Bradley et al., 2005)
Northern Host–Parasite Assemblages     9

1.2.1. Developing knowledge of parasite diversity in the North

Knowledge of parasite diversity in the North extends into the 1800s
coincidental with the earliest biological collections in Eurasia and North
America. Studies were usually local, idiosyncratic and opportunistic,
often with minimal samples providing an incomplete glimpse of parasite
diversity among a limited spectrum of vertebrate and invertebrate hosts
in terrestrial, aquatic and marine systems. A process of discovery empha-
sised taxonomy and the identification and characterisation of diverse
macroparasites and microparasites, but usually an ecosystem approach or
historical and biogeographic context was lacking.
A more comprehensive view of parasite diversity did not emerge until
cadres of scientists initiated explorations for pathogens and disease among
wildlife and at the interface for people and northern environments (e.g.
Rausch, 1972, 1974). Beginning nearly 70 years ago, a succession of parasi-
tologists and ecologists examined the triad of host–parasite environment
to advance our understanding of the structure and function of northern
host–parasite systems. Early investigations are exemplified by pioneer-
ing survey and inventory to document diversity in the Brooks Range and
other regions of Alaska in the late 1940s (e.g. Rausch, 1951, 1952, 1957,
1994) and across Eurasia and the Russian Arctic (e.g. Kontrimavichus,
1969; Gvozdev et  al., 1970; Boev, 1975; Priadko, 1976; Ryzhikov et  al.,
1978, 1979). These studies established models and baselines for defining
the structure and nature of diversity. Further, they began to recognise the
relationship of indigenous peoples on the land and their interactions with
and dependence on wildlife, through culture and subsistence food webs,
that served as determinants of parasitic infection and diseases (e.g. Babbot
et  al., 1961; Cameron and Choquette, 1963; Rausch, 1951). Classical and
elegant research in parasitology has been conducted at high latitudes, par-
ticularly that emphasising parasites transmissible to people (e.g. Rausch,
1967, 2003a). Despite a century of field-based survey and inventory, how-
ever, much remains to be revealed about the extremely diverse world of
parasitic organisms (e.g. Hoberg et al., 2003; Cook et al., 2005).
A morphologically based view of diversity that established the founda-
tions for understanding species associations and distributions (e.g. Rausch,
1952, 1957, 1976, 1994) is now increasingly complemented by molecular
approaches and discovery of considerable unrecognised diversity (both
species and populations) among most major groups of macroparasites
(e.g. Hoberg et al., 2003; Cook et al., 2005; Kutz et al., 2007; Koehler et al.,
2009; Lavikainen et  al., 2010). For example, new species and genera of
macroparasites are being discovered in such reasonably well-studied host
groups as arvicoline rodents (e.g. Rausch, 1952; Haukisalmi et  al., 2001,
2002; ­Wickström et al., 2003; Cook et al., 2005; Haukisalmi et al., 2006, 2009;
Makarikov, 2008), ungulates (Hoberg et al., 1995, 1999; Kutz et al., 2007) and
10     Eric P. Hoberg et al.

carnivores (Lavikainen et al., 2010, 2011; Haukisalmi et al., 2011), and sub-
stantial new information about host occurrence and geographic distribu-
tion has emerged (e.g. Kutz, et al., 2001b; Hoberg et al., 2002b; Jenkins, et al.,
2005; Galbreath, 2009; Durette-Desset et  al., 2010; Laaksonen et  al., 2010;
Galbreath and Hoberg, 2012). Broad integrated approaches have demon-
strated the need for both comparative morphological and molecular data
to understand patterns of cryptic parasite diversity in the North (Hoberg
et al., 2003; Pérez-Ponce de León and Nadler, 2010; Haukisalmi et al., 2011).
In the Arctic, although we have a developing understanding of spe-
cies richness and host associations, we generally lack long-term and com-
prehensive baselines for parasite biodiversity in terrestrial, aquatic and
marine systems, even for the best known host species. Absence of detailed
knowledge of parasite biodiversity has consequences for understanding
faunal structure, the role of parasites in ecosystems and patterns of emerg-
ing animal and zoonotic diseases at local to regional scales. We urgently
need to incorporate parasites into policy and management plans and to
emphasise that parasitic diseases be on the agenda for wildlife managers,
fisheries biologists and local communities. Parasitological knowledge can
be incorporated into policy and management plans through an integra-
tion of field-based survey and local knowledge, development of baselines
linked to specimens, digital data resources to assess change and predictive
spatial–epidemiological models (Hoberg et  al., 2003; Marcogliese, 2005;
Waltari and Perkins, 2010). We recommend that parasites be integrated
in the broader equations for wildlife management, particularly issues
about the sustainability of wildlife populations and subsistence food
webs including concerns for food security and food safety (zoonoses and
human pathogens) (Kutz et al., 2009b). Further, an evidence-based process
is necessary to demonstrate a clear link between climate change, environ-
mental perturbation and emergence of parasites and disease that are the
foundations for robust projections about dynamic shifts in ecosystems in
the next few decades (e.g. Hoberg et al., 2008a,b; Kutz et al., 2009b).

1.2.2. Towards an integrated picture of parasite diversity

We provide an overview of the key elements of northern landscapes, with
emphasis on high latitudes of the Nearctic (northern Canada and Alaska)
and adjacent regions of the Palaearctic (Russian Far East). In describing
the origins, history and current diversity for assemblages of mammalian
hosts and parasites, we articulate a relatively comprehensive picture for
terrestrial systems to understand faunal structure and assembly in the
North. Employing specific exemplar systems, we address the physical
and biotic processes that have served as determinants of parasite faunal
diversity in space and time. These are the foundations in part for more
detailed discussion of ungulate parasite faunas (Kutz et al., 2012) and are
Northern Host–Parasite Assemblages     11

relevant to the range of zoonoses circulating among free-ranging hosts

and people (e.g. Bradley et al., 2005; Jenkins et al., 2011). Related papers
can emphasise contemporary diversity, the dynamics of infection and dis-
ease, patterns of emergence for pathogens, population-level effects, pro-
cesses for geographic invasion from the south and the potential impact of
parasites alone and in combination with other stressors on human health
and on the sustainability of wildlife in northern ecosystems.
Exemplar systems in the North also afford the opportunity to exam-
ine conceptual issues of coevolution, historical ecology, biogeography and
invasion biology as generalities in parasite faunal diversity (e.g. Hoberg
and Brooks, 2008, 2010). A range of host–parasite assemblages illustrate
some of the current and possible future shifts in parasite and host ecology
resulting from anthropogenic change in the North. The approaches and
investigative tools used to explore these shifts are reviewed.
In a pragmatic sense, integrated studies outlined here contribute to
resolution of real-world issues in animal and human health and decisions
in wildlife management and conservation biology. Integration is essen-
tial in serving to elucidate the role of parasites, parasitism and disease
as influential factors among populations of keystone mammals, such as
ungulates, on which northern communities are dependant. We emphasise
the necessity for using systematics, biodiversity and biogeographic and
phylogeographic information as critical foundations for placing parasites
within a broader context linking host ecology and the environment (e.g.
Hoberg, 1997a,b; Avise, 2000; Brooks and Hoberg, 2000). In recent years,
the recognition of accelerating perturbation in the North, particularly
that resulting from rapid climate change, has increased these efforts (Cal-
laghan et al., 2004d; Post et al., 2009). Further, a more relevant approach to
key issues is now facilitated by the collaborative involvement of northern
communities in the development and implementation of new strategies
for the cooperative management of wildlife resources to ensure sustain-
ability in an uncertain future (e.g. Brook et al., 2009; Kutz et al., 2009b).
Beyond the functional aspects of disease and other more subtle effects
on host biology, parasites are elegant indicators of ecological structure, bio-
geography and history in complex biological systems (e.g. Brooks, 1985;
Hoberg, 1997a; Marcogliese, 2005; Nieberding and Olivieri, 2007; Waltari
et al., 2007a,b; Hoberg and Brooks, 2008, 2010; Morand and Krasnow, 2010).
Understanding parasite biodiversity contributes to addressing several fun-
damental questions about the biosphere: (1) How have faunas been struc-
tured over time? (2) Are there general rules for assembly of faunas, and are
there primary drivers for diversification in complex associations? and (3)
Can insights from historical systems (as analogues) be used in expanding
our basis for prediction related to processes and outcomes in contemporary
systems? A subset of parasite-centric questions can be further explored:
(1) How do we explain host and geographic distributions of parasites? and
12     Eric P. Hoberg et al.

(2) What are the ecological, historical and evolutionary determinants of

parasite diversity?
In northern systems, studies of parasite diversity directly complement
our knowledge about the historical processes that have served to struc-
ture faunas and the role of episodic shifts in climate that have influenced
patterns of dispersal, isolation and speciation during the late Tertiary and
Quaternary (e.g. Rausch, 1994; Hoberg, 2005a; Hoberg et  al., 2003; Cook
et al., 2005; Zarlenga et al., 2006; Waltari et al., 2007a,b; Koehler et al., 2009).
These observations highlight the idea that the ‘past is the key to the present’
with history providing a pathway or analogue for predicting how complex
host–parasite systems may respond in a regime of accelerated environmen-
tal change over time. Integration of historical processes into predictions
about a future of environmental perturbation, biotic change and shifting
patterns of species diversity is requisite (Hoberg, 1997a; Waltari et  al.,
2007b; Provan and Bennet, 2008; Galbreath et al., 2009). In a fundamental
sense, history sets the ground rules for understanding the structure of fau-
nas and the interplay of events on varying temporal and spatial scales that
have been determinants of diversity.



History and climate interact across geography as determinants of faunal

structure, an observation that emphasises the significance of drivers in evo-
lutionary time as foundations for contemporary biodiversity (Table 1.3).
Over the past 3–5 Myr of the Pliocene and Quaternary, northern systems
have been under dynamic change and these perturbations have influenced
faunas and floras on regional to landscape scales (e.g. Schweger et al., 1982;
Dynesius and Jansson, 2000; Jansson and Dynesius, 2002; Callaghan et al.,
2004a; Brochmann and Brysting, 2008; Post et al., 2009; Sandel et al., 2011).
This important role for climate represents a central axiom that underlies
our understanding of origins and patterns of diversity among complex
host–parasite systems at high latitudes across the Holarctic (e.g. Hoberg,
1992; Rausch, 1994; Hoberg et al., 2003; Waltari et al., 2007b).
Over the past 40–50 Myr, the Holarctic region linking Eurasia, the
Nearctic and Greenland represented a largely contiguous landmass with
interconnected habitats extending across high latitudes (e.g. Matthews,
1979). Substantial intercontinental expansion of mammalian faunas from
Eurasia into North America occurred near the Palaeocene–Eocene bound-
ary, about 55 million years ago (Ma), but this relatively deep history of
colonisation appears to have had minimal influence on contemporary pat-
terns of diversity in the Nearctic (e.g. Bowen et al., 2002; Beard, 2002). The
structure of contemporary faunas did not emerge until after the Miocene
Northern Host–Parasite Assemblages     13

TABLE 1.3  Generalities for structure and assembly of a complex northern fauna

Biological characteristics
• Extremes of seasonality/brief pulses of productivity, prolonged winter
• Low-diversity systems – both hosts and parasites
• Short trophic links
• Domination by limited number of taxonomic groups
• Fluctuations in abundance/population density for some host groups
○ Fluctuations in parasite abundance?
• Dense aggregation of hosts during breeding/calving
• Cryptic diversity in some parasite groups
• Adaptations for survival, resilience, transmission of parasites (taxon specific)
○ Longevity, large size, high fecundity, + rapid development, inhib-
ited development (or reduction in arrested development), multi-
year cycles, continuous transmission through winter
Historical characteristics
• Episodic climate and habitat perturbation
• Recurrent (episodic) expansion, isolation, fragmentation
• Spatial heterogeneity (refugia)
• Refugial effects, residual isolation related to vagility
• Prominent biotic filters – constraints leading to loss of diversity due to
­limited resilience/tolerances/thresholds for development and survival in
cold, xeric environments
• Prominent abiotic filters – constraints related to temperature, precipitation
and humidity
(based on Hoberg et al., 2003; Callaghan et al., 2004a; Shafer et al. 2010)

(between 23 and 5.3Ma) as otherwise equitable climatological conditions

across the region began a gradual cooling trend that culminated in the
inception of major cycles of glaciation of the Northern Hemisphere near
3.5Ma in the late Pliocene (between 5.3 and 2.6Ma) (Andersen and Borns,
1994). Subsequent to the late Pliocene, northern ecosystems developed
under a regime of dynamic climate change and episodic perturbations
of both the physical landscape and a complex biota leading to consider-
able transformation and turnover for ecological structure (e.g. Hopkins,
1959; Guthrie, 1990; Jansson and Dynesius, 2002; Callaghan et al., 2004a,d;
Guthrie, 2006). Over time through the Pleistocene (2.6Ma to 10Ka), the
fauna became increasingly Arctic-adapted and constrained by low tem-
perature and humidity.
Glaciation and vast ice sheets were the dominant theme for circumpo-
lar habitats above 60°N during the late Quaternary that encompasses the
Pleistocene and Holocene (e.g. Callaghan et al., 2004a) (Fig. 1.2). In excess of
20 glacial–interglacial cycles have been identified across the 2.6 Myr of the
14     Eric P. Hoberg et al.

FIGURE 1.2  Polar projection of the geographic distribution of continental glaciers and
glacial refugia in the Holarctic region during the last glacial maximum about 18Ka show-
ing the position of Beringia and the Bering Land Bridge. Major continental ice masses are
shown in grey, and the extent of exposed continental shelf is stippled. The Arctic Circle
(66º33′N) is indicated with a dotted line. Substantial refugial zones were present in (1)
Beringia and peripheral habitats at high latitudes of North America and eastern Eurasia,
(2) isolated zones between or within the Cordilleran and Laurentide ice sheets, including
the ice-free corridor that developed at the end of the Pleistocene, (3) along the western
coastal zone, including the Alexander Archipelago and Queen Charlotte Islands, and (4)
in periglacial habitats south of the ice sheets. This figure was produced based on infor-
mation presented by Pielou (1991), Dyke et al. (2004), Harington (2005) and Shafer et al.
(2010) and modified from Hoberg et al. (in press-a).

Pleistocene; during the late Pliocene and early in the Pleistocene, these oscil-
lations occurred on roughly 41 thousand year (Kyr) cycles, which shifted to
100 Kyr episodes after about 800Ka (Muller and MacDonald, 1997; Jansson
and Dynesius, 2002). During recurrent glacial maxima, substantial reduc-
tions in sea level (−120m lower than contemporary levels) exposed areas
Northern Host–Parasite Assemblages     15

of continental shelf allowing biotic expansion between Eurasia and North

America (Hopkins, 1959). Continental glaciation partitioned habitats, partic-
ularly in the Nearctic. Glaciation was not universal and critical ice-free zones,
or refugia with considerable implications for faunal structure and continuity
(Fig. 1.2), existed in high latitudes of Asia and North America (e.g. Haring-
ton, 2005; Shafer et al., 2010). In North America, refugial zones occurred at
varying temporal and spatial scales including habitats north and south of
the Laurentide–Cordillera ice sheets, at fine scales in the borderlands of these
continental glaciers, along the northwestern coastal zones and apparently in
the high Arctic (Rand, 1954; Callaghan et al., 2004a; Shafer et al., 2010).

1.3.1. Exploring the Beringian connection

Cyclical processes for alternating episodes of glacial advance and reces-
sion had a pervasive influence on the distribution and structure of floras
and faunas across the region (e.g. Andersen and Borns, 1994; Jansson and
Dynesius, 2002; Abbott and Brochmann, 2003). Drivers for diversity and
structure across the circumpolar north are exemplified by processes iden-
tified in Beringia and adjacent regions of the Nearctic where the dynamics,
patterns and consequences of episodic change are particularly evident at
both intercontinental and regional–intracontinental scales (e.g. Fedorov
and Stenseth, 2002; Galbreath and Cook, 2004; Galbreath et  al., 2009;
Shafer et al., 2010). The geographic limits of Beringia have been defined
in a variety of ways to emphasise different geologic and biogeographic
aspects of the region spanning eastern Siberia and northwestern North
America (Harington, 2005) (Fig. 1.3). As first envisioned by Hultén (1937),
who described the region based on phytogeographical evidence, Beringia
encompassed the area between Russia’s Lena River (125°E) and Canada’s
Mackenzie River (130°W). Later authors distinguished between broad and
narrow geographic designations. For example, Yurtsev’s ‘Megaberingia’
(1974) and Sher’s ‘Beringida’ (1984) placed the western boundary of the
region at the Taimyr Peninsula (100°E) or further west, but both authors
also described more narrowly delineated Beringian zones centred around
the Bering Isthmus and Strait. The Great Beringia concept of Yurtsev
(1974) places the western boundary at the Kolyma River (160°E), which
is consistent with a growing body of comparative phylogeographic evi-
dence showing genetic discontinuities in the same area (Hewitt 2004a,b).
Beringia, as a faunal province during the Pleistocene, was thus the
nexus or crossroads for the northern continents. Steppe landscapes dur-
ing glacial maxima were a filter bridge for biotic expansion out of Eurasia
for a diverse terrestrial fauna (Hopkins, 1959, 1967; Kontrimavichus, 1976;
Hopkins et  al., 1982; Pielou, 1991; Sher, 1999; Waltari et  al., 2004, 2007b;
Elias and Crocker, 2008) and for human colonisation of North America
(Dixon, 2001; Hoffecker et al., 1993). Further, Beringia served as the primary
16     Eric P. Hoberg et al.

FIGURE 1.3  Geographic region of the Bering Land Bridge and maximal extent of Late
Pleistocene glaciations in Beringia about 18Ka (from Galbreath and Cook, 2004). The
Kolyma Uplands are a putative historical barrier that may have further defined the
borders of western Beringia. During episodic glacial stages from the Pliocene through
the termination of the Pleistocene, Beringia served as the gateway for expansion by a
terrestrial biota from Eurasia into North America.

intersection for marine exchange between the Atlantic and Pacific basins
via the Arctic Ocean during interglacial periods (e.g. Vermeij, 1991; Hoberg,
1992). This province has been critical for the origins and maintenance of
an arctic-adapted fauna, as a primary dispersal corridor and as a source
region that has influenced the continuity of the Holarctic biota (Guthrie and
Matthews, 1971; Hopkins et  al., 1982; Rausch, 1994; Hoberg, 1995; Sher,
1999; Repenning, 2001; Hoberg, 2005a; Waltari et al., 2007b).
Episodic faunal expansion, geographic colonisation and cycles of isola-
tion have occurred at different modes and tempos extending from the late
Tertiary through the Quaternary in response to fluctuations in climate and
shifts in environmental and ecological structure (e.g. Hoberg, 1992; Rausch,
1994; Hoberg, 1995; Lister, 2004; Waltari et al., 2004, 2007b; Hoberg 2005a;
Galbreath, 2009; Koehler et al., 2009). Biotic expansion in terrestrial systems
has been predominately asymmetrical, involving eastward dispersal from
Eurasia into the Nearctic as evidenced by diverse assemblages of mammals
(soricomorphs to ungulates) and their associated micro- and macroparasite
faunas (Waltari, et al., 2007b). Ecologically and phylogenetically disparate
terrestrial faunas including nematodes in lagomorphs and artiodactyls
(Hoberg, 2005a; Durette-Desset et  al., 2010), helminths inhabiting carni-
vores (Rausch, 1994; Zarlenga et al., 2006; Koehler et al., 2009; Haukisalmi
Northern Host–Parasite Assemblages     17

et  al., 2011), the cestodes infecting arvicoline rodents and Ochotonidae
(Haukisalmi et al., 2001; Wickström et al., 2003; Cook et al., 2005; Haukisalmi
et al., 2006; Galbreath, 2009; Galbreath and Hoberg, 2012; Makarikov et al.,
in press) all exhibit general patterns of episodic biotic expansion and iso-
lation between the Palaearctic and Nearctic (and at fine intracontinental
scales) at specific times during the late Tertiary and Quaternary (Fig. 1.4).
Adjacent Beringian marine biotas exhibit complementary patterns linking
the Atlantic, Arctic and North Pacific basins within similar temporal limits
(e.g. Hoberg, 1992, 1995; Hoberg and Adams, 2000; Hoberg et al., 2003).



Beringian parasite assemblages, both marine and terrestrial, represent

elegant exemplars for exploring the intricacies of geographic colonisa-
tion in shallow evolutionary time (Hoberg, 1992, 1995; Rausch, 1994;
Haukisalmi et al., 2001; Hoberg et al., 2003; Wickström et al., 2003; Cook
et al., 2005; Haukisalmi et al., 2006; Zarlenga et al., 2006; Waltari et al.,
2007b; Galbreath, 2009; Koehler et al., 2009). It is evident, however, that
considerably broader phylogeographic inference has been achieved
for recognised mammalian host groups than for many of the specific
host–parasite assemblages (Waltari et  al., 2007b; Shafer et  al., 2010).
In northern systems, much remains to be discovered relative to basic
issues of biodiversity (species richness and distribution) and the struc-
ture and development of faunal associations (Hoberg et al., 2003; Cook
et al., 2005; Waltari et al., 2007b). We explore a series of four exemplar
assemblages that represent phylogenetically and ecologically disparate
mammalian groups and their parasites in terrestrial environments to
demonstrate general and specific patterns for the history of faunal asso-

1.4.1. Faunas associated with terrestrial Carnivora

• The parasite groups: Cestoda – Cyclophyllidea, Taeniidae (Taenia,
Echinococcus); Diphyllobothriidea (Diphyllobothrium); Nematoda –
Ascaridida (Baylisascaris, Toxascaris); Strongylida, Ancylostomatoidea
(Uncinaria), Molineoidea (Molineus); Enoplida, Dioctophymatoidea
(Soboliphyme), Trichinelloidea (Trichinella) (Table 1.4).
• The host groups: Carnivora – Canidae (Canis, Vulpes), Felidae (Lynx),
Mustelidae (Mustela, Martes, Gulo), Ursidae (Ursus).
• Taxonomy for hosts is consistent with Wilson and Reeder (2005). Tax-
onomy for nematodes is consistent with Anderson (2001); for cestodes,
it is based on Kahlil et al. (1994) with modifications proposed by Kuchta
et al. (2008).
18     Eric P. Hoberg et al.

FIGURE 1.4  History for geographic expansion by phylogenetically disparate host–

parasite assemblages from Eurasia to the Nearctic through the Beringian region
superimposed on a view of the circumpolar region during maximum reduction in sea
level. Geographical colonisation in terrestrial systems and faunas was asymmetrical
and characterised by episodic expansion in the amphiberingian region that extended
­temporally from the Pliocene through the Pleistocene. These events directly ­influenced
patterns of diversity and occurrence for some helminth taxa among terrestrial
­(carnivorans, lagomorphs, rodents, artiodactyls and soricomorphs) and marine ­mammals
(pinnipeds). The history for most host–parasite assemblages in terrestrial systems relates
to origins in Eurasia and eastward expansion across Beringia into the Nearctic region
(indicated by the directionality of the solid arrows); there is minimal evidence for a west-
ward pattern of expansion or interchange (dotted arrows). The distribution of marine
systems complements those on land, where Beringia and the land bridge alternately
served as pathway or as a barrier to biotic expansion depending on prevailing climate
and sea levels. Map projection and figure is modified from Hoberg and Brooks (2010).
Northern Host–Parasite Assemblages     19

Contemporary groups and species with protracted histories in north-

ern systems are recognised within four clades of terrestrial carnivorans
(Kurtén and Anderson, 1980); a subclade containing Felidae and Hyaeni-
dae (feliforms) are the sister of subclades (caniforms) including Canidae,
Ursidae + Pinnipedia and Mustelidae + Procyonidae (Bininda-Emonds
et al., 2007; Nyakatura and Bininda-Emonds, 2012). Eurasian associations,
extending to the Oligocene (34–23Ma) and Eocene (56–34Ma) and earlier,
are noted for groups that are now distributed at high latitudes of North
America and the Holarctic (Kurtén and Anderson, 1980; Beard, 2002). The
Tertiary history for carnivorans has been strongly influenced by patterns
of episodic extinction, turnover and ecological replacement (Van Valken-
burgh et al., 2004). Some carnivorans, particularly canids, radiated exten-
sively in the Nearctic, but only Caninae persisted to the present and their
history extending into the Holocene links Eurasia and North America.
Multiple expansion events (both among and within certain taxa) into the
Nearctic (and to a lesser extent the Palaearctic) during the Miocene, Plio-
cene and Pleistocene established the distributions for modern taxa and
extant species assemblages (e.g. Kurtén and Anderson, 1980; Waits et al.,
1998; Vilà et al., 1999; Stone and Cook, 2002; Johnson et al., 2006; Waltari
et al., 2007b; Koepfli et al., 2008; Aubry et al., 2009); notably, Hyaenidae
also expanded from Eurasia into North America but the family is poorly
represented in the fossil record.
Events of geographic colonisation involve a number of host genera,
but relatively few species now have Holarctic distributions; the latter
include ermine (Mustela erminea), least weasel (M. nivalis), wolverine
(Gulo gulo), Arctic fox (Vulpes lagopus), red fox (V. vulpes), wolf (Canis
lupus), brown bear (Ursus arctos) and polar bear (U. maritimus). Helminth
parasite faunas encompass elements that are both specific to particular
carnivoran groups and shared based on biogeographic history, ecologi-
cal similarity, foraging behaviour and guild associations (e.g. Kontrima-
vichus, 1969; Rausch, 1994; Hoberg, 2006). Faunal structure is further
influenced by the timing, extent and number of expansion and isola-
tion events primarily during the Pliocene and Quaternary (Vilà et  al.,
1999; Waltari et al., 2007b) within this phylogenetically and ecologically
disparate assemblage of Carnivora (e.g. Bininda-Emonds et  al., 2007;
Koepfli et  al., 2008; Nyakatura and Bininda-Emonds, 2012). Further,
changing patterns of diversity, degrees of sympatry, extinctions and fau-
nal turnover among carnivoran hosts as exemplified at intercontinental
scales and regionally in eastern Beringia may have also influenced the
occurrence of various parasite taxa (Youngman, 1993; Rausch, 1994; Van
Valkenburgh et al., 2004). In a contemporary setting, distributions and
ecological characteristics, particularly prey species and foraging pat-
terns, for carnivorans and their assemblages of parasites are among the
primary determinants or limiting factors for a number of potential and
TABLE 1.4  Species diversity and biogeography for exemplar helminth parasites among Carnivora in the Arctic and Subarctic, exploring

­assemblages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected
for global diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic

Parasite taxon Host association Distribution Species diversitya Processesb

Eric P. Hoberg et al.

Taenia spp. Mustelidae, Canidae, Holarctic/Beringian (45G/15H/5N/25P) GE, HC
­Felidae, Ursidae (9 amphiberingian)
Echinococcus spp.c Canidae Holarctic/Beringian (10+G?/2H?/0N/6+P) GE
Diphyllobothrium spp. Canidae/Ursidae Holarctic/Beringian (50+G/11+H/3+N/16+P) GE, HC
Mesocestoides spp. Carnivora Holarctic/Beringian (12+G/2H/3N/8P) GE, HC
(2 amphiberingian)
Molineus sp.d Mustelidae/Canidae/­ Holarctic/Beringian (16+G/1H/3N/5P) GE, HC
Uncinaria spp. Ursidae/Canidae Holarctic/Beringian (14+G/3H/2N/4P) GE, HC
Baylisascaris spp. Canidae/Mustelidae/­ Holarctic/Beringian (7+G/2H/3N/1P) GE
Toxascaris Carnivora Holarctic/Beringian (3+G/1H/0N/2P) GE
Trichinella spp. Carnivora Holarctic/ Beringian (12G/1H/2N/8P) GE, HC
Soboliphyme spp.e Mustelidae Holarctic Beringian (9G/2H/0N/7P) GE, HC, R
a  Species diversity relative to regions: G = global, H = Holarctic, N = Nearctic, P = Palaearctic.
b  Processes include geographic expansion = GE; host colonisation = HC; refugial effects = R.
c  Echinococcus systematics remain in flux. There are 10 putative species recognised. Two endemic species are distributed in the Neotropical region; no species are

known to be endemic to North America. Aside from the Holarctic E. multilocularis and ‘E. granulosus’ all other known species occur in the Old World (see Nakao
et al., 2007).
d  Primary diversity for Molineus is found in the tropics of southern Asia and in the Neotropical region. The single Holarctic species has a broad distribution among

e  T he genus Soboliphyme includes nine species, eight of which occur as parasites in soricomorphs; S. baturini is the only species in carnivore definitive hosts and is one

of two Holarctic species (Koehler et al., 2009).

Northern Host–Parasite Assemblages    

22     Eric P. Hoberg et al.

recognised zoonotic protozoans, tapeworms and nematodes that can

­circulate in human hosts (e.g. Rausch, 1956, 1994; Rausch and Fay, 2011).
Mustelids have a relatively long trans-Beringian history with successive
expansion events into the Nearctic occurring over extended time frames
and during different intervals beginning in the late Miocene (Kurtén and
Anderson, 1980; Koepfli et al., 2008). Diversification and assembly of the
extant high-latitude fauna, composed of weasels (Mustela spp.), fisher (Mar-
tes pennanti), wolverine and martens (Martes spp.), have resulted from a
minimum of four independent events of geographic colonisation into North
America during the Pliocene and Pleistocene. Refugial effects in periglacial
habitats north and south of the Laurentide–Cordillera systems and in the
western coastal zone along with patterns of secondary expansion appear
as important determinants for diversification and distribution among two
species of martens, M. americana and M. caurina, in North America (Stone
and Cook, 2002; Stone et al., 2002). Martens demonstrate distinct patterns
of divergence between continental and coastal refugial populations. In con-
trast, there is only one species of wolverine across the Holarctic. In North
America, genetic divergence, although minimal, indicates endemic wolver-
ine populations occupying Southeast Alaska, the Kenai Peninsula and the
central Canadian Arctic, reflecting dispersal from Beringia following the
termination of the Pleistocene (Tomasik and Cook, 2005). Weasels (Mustela
spp.) represent yet another expansion event into North America from the
Palaearctic across Beringia (Fleming and Cook, 2002).
Felids have a deep history across the Holarctic, initially being recog-
nised in the faunas of Eurasia and North America near the Eocene–­
Oligocene boundary (Kurtén and Anderson, 1980). Contemporary felid
lineages, however, have initial origins linked to Eurasia and the divergence
of large cats, with this region serving as a source area for later colonisation
of Africa and the Nearctic (Johnson et al., 2006). Expansion across Berin-
gia occurred in the Miocene (about 8.0–8.5Ma) leading to establishment
and radiation of three extant lineages (ocelot, lynx and puma), only one
of which (Lynx) has had continuity at high latitudes (Johnson et al., 2006).
Secondarily, North America served as a centre of diversification for felids,
with dispersal events into South America (ocelot), and Eurasia (cheetah,
lynx) during the Pliocene. Large cats in the Panthera lineage, including
lions, attained exceptionally broad geographic distributions in the Pleisto-
cene, which extended from South America to Eurasia and Africa across the
Bering Land Bridge (Kurtén and Anderson, 1980). Panthera leo persisted in
Beringia late into the Wisconsinan and would have represented an impor-
tant component of a complex fauna of mega- and mesocarnivores. The
contemporary Lynx canadensis occurs across the boreal forest zones of the
Nearctic and is sporadically present on the tundra coinciding with periods
of high abundance for snowshoe hare (Lepus americanus) (MacDonald and
Cook, 2009).
Northern Host–Parasite Assemblages     23

Canidae arose in the Eocene–Oligocene of North America and Eurasia

and radiated extensively through the Miocene with considerable diversity
now characterising the global fauna (Nowak, 1999; Bardeleben et al., 2005).
Beringia figured prominently as a gateway into the Nearctic and in some
cases downstream to the Neotropical region, although only three species
among the Caninae or true dogs and foxes now occur at high latitudes
(Kurtén and Anderson, 1980). Broad distributions in the Holarctic are known
for grey wolf (C. lupus), red fox (V. vulpes) and Arctic fox (V. lagopus). Domestic
dogs (C. lupus familiaris) are also considered within this assemblage.
Although wolves appeared in North America by 2Ma, the grey wolf
(as a putative descendant of C. etruscus) has origins in Eurasia about
700Ka with first occurrences in the Nearctic via the Bering Land Bridge
by the middle Pleistocene (Kurtén and Anderson, 1980; Vilà et al., 1999).
Wolves were well represented among carnivore faunas of eastern Berin-
gia as highly vagile predators capable of dispersing over considerable
distances (Guthrie, 1968a). There is evidence of multiple expansion
events from Eurasia into North America during glacial stages over the
late Pleistocene, with ranges subsequently extending far to the south
during interglacials (Vilà et al., 1999). Notably, wolf populations occupy-
ing former coastal refugial zones are genetically distinct from those with
broader continental distributions, indicating effective barriers to gene
flow over the late Pleistocene (Weckworth et  al., 2005). Recurrent pat-
terns for episodic expansion, however, have often obscured population
structure and history and constitute factors that likely influenced species
and genetic diversity for parasites associated with these large carnivores.
Dogs at high latitudes are initially recognised in fossil assemblages dat-
ing to near 20Ka in eastern Beringia (e.g. Kurtén and Anderson, 1980).
Red fox, in contrast, initially arrived in North America during the
Illinoian glaciation (130–200Ka) or earlier. During the Sangamon, interglacial
(110–130Ka) foxes occurred in forested habitats at temperate latitudes with
isolated populations, leading to discrete eastern and western clades, dis-
tributed south of the Laurentide during the Wisconsinan (about 110–12Ka)
(Aubry et  al., 2009). Foxes representing this early colonisation of North
America became extinct in Beringia and were later replaced by those of
Eurasian origin during the middle Wisconsin. In North America, foxes now
occur as isolated populations of disparate ages and ancestry: (1) endemic
populations (montane and eastern subclades) and their descendents that
have been resident since at least the Illinoian and (2) a Holarctic lineage
composed of populations with Eurasian ancestry that expanded into east-
ern Beringia during the Wisconsinan and eventually south and east as far as
Alberta and the Northwest Territories at the termination of the Pleistocene
(Aubry et al., 2009). Further, foxes have been extensively translocated in the
last century such that populations may now include admixtures (mosaics)
of exotic introduced animals and endemics at some localities. These patterns
24     Eric P. Hoberg et al.

may have particular implications for the distribution of such zoonotic para-
sites as Echinococcus multilocularis and Taenia crassiceps. For example, it is not
clear whether or not all red foxes (irrespective of ancestry and origin) (1) are
equally susceptible to infections by these taeniids, (2) have been components
of larger assemblages of canid hosts and parasites or (3) if secondary contact
and host switching have occurred over time.
Arctic foxes are related to an assemblage of red fox-like canids with ori-
gins in Eurasia during the Villafranchian (1–3Ma, bordering the late Plio-
cene and lower Pleistocene). These foxes secondarily expanded across the
circumpolar region during the Wisconsinan (Kurtén and Anderson, 1980;
Rausch, 1994; Bardeleben et  al., 2005) and are highly adapted to harsh
frigid and xeric conditions that characterise high-latitude tundra, coastal
and pack ice habitats. In contrast to a broad assemblage of terrestrial mam-
mals, glacial events in the Quaternary did not serve as isolating mecha-
nisms for Arctic fox (Dalén et al., 2005). Foxes were isolated in response
to warming conditions and persisted in high Arctic refugia during the last
interglacial (Sangamon, ending about 117Ka) and subsequently underwent
rapid population and geographic expansion to become widely distributed
in Wisconsinan time across the circumpolar region. Extensive contempo-
rary gene flow is related to long-range dispersal in circumpolar habitats
for arctic fox and little population differentiation has been demonstrated
(Dalén et al., 2005). Across this region, two ecotypes are recognised includ-
ing a ‘lemming’ morph that targets Lemmus and Dicrostonyx as primary
prey (Eurasia, North America, Canadian Archipelago and East Greenland)
and ‘coastal’ adapted forms (Svalbard, Iceland, west Greenland) that for-
age nearshore on birds, eggs and carrion. Such differences in foraging and
distribution may influence the patterns of occurrence of E. multilocularis
and its relationship to potential human infections (Henttonen et al., 2001).
The bears, Ursidae, have a complex history linking Eurasia and North
America, with evidence of multiple expansion events into the Nearctic over
the late Tertiary and Pleistocene (Talbot and Shields, 1996a; Yu et al., 2004).
Tremarctine bears (species of Tremarctos and Arctodos) radiated in North
America but are now represented only by the spectacled bear (T. ornatus)
in South America. Ursine bears radiated initially in the Palaearctic and
include three species (black bear, Ursus americanus; brown bear, U. arctos,
and polar bear, U. maritimus) with independent histories in North America
(Kurtén and Anderson, 1980). Tremarctine and ursine bears would have
been contemporaneous and sympatric at localities in Beringia and south of
the Laurentide during the Pleistocene (Kurtén and Anderson, 1980).
Black bears have origins in Eurasia during the Pliocene, and U. ameri-
canus was widely distributed in North America by the mid-Pleistocene in
localities south of the Laurentide (Kurtén and Anderson, 1980). Contem-
porary black bears appear to be immigrants from the south, arriving in
the former Beringian refugium and at higher latitudes in North America
during the Holocene (Guthrie, 1968a). Distinctive lineages for coastal (SE
Northern Host–Parasite Assemblages     25

Alaska) and continental populations are now recognised (e.g. MacDon-

ald and Cook, 2009), consistent with an extended history of occupation in
nearshore refugia during the Pleistocene (Heaton and Grady, 2003).
Brown bears have origins in Eurasia during the Villafranchian but are
not seen in eastern Beringia and North America until the early Wisconsinan,
although this species may have been more widespread to the south of the
Laurentide prior to the late glacial stages of the Pleistocene (MacDonald
and Cook, 2009). The distribution of genetic diversity for brown bears in
the Nearctic is consistent with a complex history involving multiple expan-
sion events across Beringia and patterns of refugial isolation during glacial
maxima (Heaton and Grady, 1993; Waits et  al., 1998; Heaton and Grady,
2003). Similar to black bears, there has been recognition of genetically dis-
tinct coastal and continental populations of brown bear in North America,
highlighting the importance of former refugial zones in the Alexander
Archipelago of SE Alaska (Talbot and Shields, 1996b; Waits et al., 1998).
Polar bears are closely related to brown bears, and it was thought that
origins extended no deeper than the late Pleistocene about 150 Ka (Shields
and Kocher, 1991; Lindqvist et al., 2010). Revision of this date toward the
middle Pleistocene near 600 Ka (Hailer et al., 2012) now suggests that diver-
gence from a common ancestor with brown bears may be related to expan-
sion of perennial sea ice in the Arctic Ocean about 700 Ka (Herman and
Hopkins, 1980). Thus the structure and linkages within the Arctic Ocean
ecosystem were firmly established at that time. Further, a history of diver-
sification extending to the middle Pleistocene implies these highly adapted
Arctic marine carnivores have persisted across multiple glacial-interglacial
cycles through the late Quaternary. as is apparent for some other high
­latitude mammals (Lister, 2004). These bears are highly vagile, obligate car-
nivores (usually apex predators of marine mammals) primarily associated
with open ice pack and high-latitude tundra environments around the cir-
cumpolar region. Individuals are wide ranging over long distances, as indi-
cated by minimal differentiation among populations around the Arctic basin
(e.g. Peatkau et al., 1999). Similar to Arctic foxes, extensive travel by polar
bears may serve to mediate gene flow for some parasites, such as Trichinella
nativa, that circulate in an assemblage of high-latitude carnivores in marine
and terrestrial environments. Interestingly, the helminth fauna of polar
bears is limited, reflecting to some extent a specialized diet of pinnipeds
and carrion, and a relatively extended association with offshore marine
environments over the terminal Quaternary. Trichinella and carnivorans

Species of Trichinella circulate in sylvatic cycles among guilds of mesocarni-
vores (felids, canids and mustelids), ursids, some pinnipeds and an array of
omnivorous prey species including rodents and soricomorphs in the Palaearc-
tic and Nearctic (Pozio 2005; Pozio et  al., 2009). Carnivory and scavenging
26     Eric P. Hoberg et al.

FIGURE 1.5  Biogeographic history for species of Trichinella (T1–T12), following origins in
Eurasia and periods of expansion through Beringia and other regions. The current species
phylogeny for Trichinella is mapped to show the history of distribution (modified from
Pozio et al., 2009). A single species, T. nativa (T2), has a Holarctic distribution, whereas
two others endemic to North America (T. murrelli – T5, and T6) have origins subsequent
to episodes of geographic colonisation by carnivores from Eurasia during the Pleisto-
cene. The occurrence of T12 is attributed to trans-Beringian expansion with felids into
South America during the Miocene. These patterns demonstrated for Trichinella serve
as a primary exemplar for the process of geographic invasion and its influence on faunal
structure and diversification in a variety of other host–parasite assemblages in phyloge-
netically diverse mammals in terrestrial systems.

represent the primary routes for transmission and have been central to pro-
cesses of diversification associated with patterns of host switching and geo-
graphic colonisation. Among encapsulated forms, there are currently nine
designated genotypes or named species (Pozio et  al., 2009). Biogeography
and radiation for species of Trichinella in carnivoran (feliforms and caniforms)
and other mammalian hosts have involved high-latitude regions of the Hol-
arctic since the Miocene (Zarlenga et al., 2006; Pozio et al., 2009). Following
initial diversification in Eurasia, four discrete events for biotic expansion into
the Western Hemisphere occurred across the Bering Land Bridge (Fig. 1.5)
influencing five species among the nine recognised genotypes: (1) through the
Nearctic to the Neotropical region during the late Miocene with an early felid
lineage prior to the emergence of the Panamanian Isthmus resulting in the T12
genotype; (2) multiple isolation events in North America from an Holarctic
assemblage near the Pilocene–Pleistocene boundary (2.5–3.0 Ma) leading to T.
murrelli (T5, in temperate to boreal zones) and later divergence of T. nativa (T2,
southern limit defined by the January – 4°C isotherm) and the genotype T6
Northern Host–Parasite Assemblages     27

(boreal to Subarctic) near 400–500Ka and (3) origin of the genotype T9 in Japan
either by expansion from the Nearctic or by peripheral isolation within the
crown group of Trichinella. The contemporary distribution for Trichinella nem-
atodes in mustelids, ursids, canids and other carnivores provides evidence
for the role of extensive host switching (driven by the dynamics of foraging
guilds) and episodic expansion out of Eurasia (Zarlenga et  al., 2006; Pozio
et al., 2009). Temporal estimates for arrival of mustelids, some canids and bears
in the Nearctic, as outlined previously, appear to coincide with the ­history for
diversification of this assemblage of Trichinella at high latitudes. Geographic
distributions and patterns of speciation were further determined by refugial
effects at inter- and intracontinental scales (e.g. relative to the Laurentide and
Cordillera ice masses) (Pozio et al., 2009). Mosaic faunas are apparent where
species resulting from independent processes of geographic colonisation dur-
ing the Quaternary are circulating in sympatry following secondary expan-
sion in the Holocene across regional settings and at some localities.
At high latitudes, the freeze-resistant T. nativa is the primary source for
infections in people, through consumption of bears and walrus (Odobenus
rosmarus), although a broad array of mammals may be infected (Dick and
Pozio, 2001). Polar bear, wolverine and Arctic foxes may be particularly
important in maintaining a broad geographic range for the parasite. Genetic
structure for T. nativa may parallel that demonstrated among the highly
vagile hosts involved in circulation, where considerable levels of gene flow
mediated by polar bears and Arctic foxes in the circumpolar region would
be predicted.
Historically, Trichinella has been part of the landscape in northern sys-
tems, representing a primary zoonotic parasite possibly recognised since
arrival of the first human immigrants from Eurasia. For example, tradi-
tionally in Alaska, meat from bears is not consumed raw but is always
cooked due to the threat of infection by these nematodes (Rausch, 1972).
Accelerated climate change in northern systems is now predicted to drive
shifts in the distribution of Trichinella spp. as the structure of marine food
chains is altered over time leading perhaps to increased levels of exposure
to infections for people (Rausch et al., 2007). Soboliphyme baturini in Mustelidae

Among nine species of Soboliphyme, seven occur as parasites of soricomorph
definitive hosts (both shrews, Soricidae, and moles, Talpidae) from Eurasia,
whereas single species occur, respectively, in a soricid from the Nearctic and
in small to medium carnivorans from northeastern Eurasia and ­northwestern
North America (Ribas and Casanova, 2006; Karpenko et al., 2007; Koehler
et al., 2007). A broad distribution in Palaearctic soricomorphs appears consis-
tent with radiation for this parasite group in Eurasia, with secondary expan-
sion into North America during the Pliocene and Quaternary.
28     Eric P. Hoberg et al.

Soboliphyme baturini, a characteristic large nematode occurring in the stom-

ach of mustelids, and occasionally other mesocarnivores, is a primary para-
site among species of Martes with a geographically widespread range centred
on the amphiberingian region (landmasses encompassing greater Beringia
in the Nearctic and Palaearctic) (Kontrimavichus, 1969; Koehler et al., 2007).
Transmission is dependent on a complex lifecycle involving ­oligochaete first
intermediate hosts, and soricomorph, or less often arvicoline, paratenic hosts
(Karmanova, 1968; Karpenko et al., 2007; Koehler et al., 2007).
The history for S. baturini contrasts with species of Trichinella in that a
narrow spectrum of congeneric host species has been involved in bioge-
ography and evolution of the assemblage. Gene flow, patterns of isolation
and population structure are mediated by relatively few host species for S.
baturini, whereas guild dynamics and a phylogenetically disparate array of
carnivorans and omnivores with varying levels of vagility characterise Trich-
inella (Zarlenga et al., 2006; Koehler et al., 2009). Soboliphyme baturini provides
insights about geographic expansion and isolation as drivers for the Nearctic
fauna. Phylogeographic analyses exploring sequence data from multigene
systems demonstrated a relatively shallow history with minimal diversifi-
cation (Koehler et  al., 2009). Population structure revealed for parasites is
related to geographical and physical events rather than cospeciation linked
to hosts and host phylogeny (Koehler et al., 2009; Hoberg et al., in press a).
Subsequent to an origin in Eurasia, geographical expansion and col-
onisation by S. baturini extended eastward across Beringia into Alaska
with the ancestor of M. caurina + M. americana as early as 1Ma during a
middle Pleistocene glacial cycle (Stone et  al., 2002; Koepfli et  al., 2008).
As of the late Pleistocene, coincidental with the early maximum of the
terminal Wisconsin glacial cycle 65–122Ka, these two species of martens in
North America were distributed south of the Cordillera and Laurentide in
western (M. caurina) and eastern (M. americana) refugia (Stone et al., 2002).
Although host speciation occurred over this million years of divergence,
similar patterns for diversification of Soboliphyme are not recognised, and
the associations of S. baturini with M. caurina and M. americana represent a
complex temporal and spatial mosaic.
Phylogenetic and phylogeographic structure for Soboliphyme is consis-
tent with geographic colonisation from Eurasia across Beringia and an ini-
tial north to south expansion with sequential isolation in insular (SE Alaskan
archipelago) and coastal refugial zones extending along the western shore
of North America. Relatively extensive genetic diversity in coastal popula-
tions of S. baturini indicates an extended period of geographic occupation
and persistence of the assemblage in putative ice-free refugial zones for hosts
and parasites leading up to the terminal Wisconsinan (Koehler et al., 2009).
Parasite populations in the coastal zone are represented by a mosaic of older
endemics (with extensive and local genetic variation), more recently derived
colonisers (where genetic diversity is not strongly partitioned geographi-
cally), and translocated or introduced populations that have discordant
Northern Host–Parasite Assemblages     29

histories relative to geography (Hoberg et al., in press-a). In these instances,

parasites serve as robust indicators with genetic signals that demonstrate
complex histories for persistence of endemic populations, secondary zones of
contact and the influence of anthropogenic translocation on faunal structure. Taenia tapeworms and carnivorans

Species of Taenia are obligate parasites of carnivores and depending on
the species involved have rodents, lagomorphs or ungulates as interme-
diate hosts; complex life cycles are directly defined by predator–prey rela-
tionships (Loos-Frank, 2000; Hoberg, 2006). Approximately 45+ species
occur in the global fauna, with 13 distributed at high latitudes among
mustelids, canids, felids and ursids across the Holarctic (e.g. Rausch,
1994, 2003b; Lavikainen et  al., 2010, 2011; Haukisalmi et  al., 2011). Sys-
tematics for Taenia is in a state of flux, with increasingly robust sampling
now becoming available that will support testing of current phylogenetic
hypotheses (e.g. Hoberg, 2006; morphological) based on multi-locus
molecular data (e.g. Lavikainen et al., 2008).
Among mustelids, four species of Taenia occur in Martes spp. (T. interme-
dia across the Holarctic; T. martis in Eurasia), G. gulo (T. twitchelli, Holarctic)
and Mustela spp. (T. mustelae, Holarctic) (Rausch 1977, 1994, 2003b). Excluding
T. mustelae, these species form a subclade of taeniids that primarily occur in
mustelid hosts (Hoberg, 2006). Taenia intermedia is a typical tapeworm among
Pacific and American marten and fisher from North America and in sable from
eastern Siberia. Taenia twitchelli is a specific cestode of wolverines and exhibits
an amphiberingian distribution linking the Nearctic and Palaearctic. Coinci-
dental with the host group, these distributions demonstrate a history of inde-
pendent expansion across Beringia from Eurasia with subsequent isolation in
the Nearctic during the Pliocene and Pleistocene. More broadly, the host distri-
butions reflect a deep coevolutionary association as suggested by sister group
relationships linking the Procyonidae, Mustelidae and their specific species of
Taenia (e.g. Hoberg 2006; Bininda-Emonds et al., 2007; Nyakatura and Bininda-
Emonds, 2012). In contrast, as the putative basal species in the genus, T. muste-
lae has broader host associations including martens and small mustelids such
as ermine, least weasel and mink (Neovison vison). An extensive range across
the Holarctic suggests a deep history extending to the Pliocene and some
level of host switching reflecting the importance of guild dynamics among an
assemblage of small carnivores as a determinant of parasite distribution.
Among canids, species of Taenia are characteristic in wolves
(T. hydatigena, T. krabbei with ungulate intermediates) and in both Arctic
fox and red fox (T. polyacantha, T. crassiceps with rodent intermediates). At
high latitudes, T. krabbei is also found in Arctic fox in both Greenland and
Svalbard. Holarctic distributions for these assemblages were apparently
attained during the Pleistocene following expansion across Beringia and
circumpolar habitats.
30     Eric P. Hoberg et al.

Considering foxes, T. polyacantha includes Eurasian (T. p polyacantha,

south of the tundra zone in red fox) and circumpolar subspecies (T. p. arctica,
Holarctic in Arctic fox and uncommon in red fox) (Rausch and Fay, 1988).
In the Nearctic, T. p. arctica is not found south of the tundra zone in red fox
(Rausch and Fay, 1988), thus it would not be expected in endemic mon-
tane or eastern clade foxes. This geographic pattern suggests that Arctic fox
and lemmings may maintain this cestode at high latitudes in the Nearctic.
This pattern may contrast with the distribution of T. crassiceps that is more
widespread in red foxes at boreal latitudes in North America. This taeniid is
known in Arctic fox and has been documented in eastern clade red fox, but
not apparently in montane foxes. Interestingly, constraints on distribution
for these taeniids may be linked to ranges occupied by arvicoline rodents
as intermediate hosts, and post-Pleistocene expansion at high latitudes may
have been initially limited by voles and lemmings (Myodes rutilus and Lem-
mus trimucronatus) and the availability of deglaciated habitats (Rausch, 1994).
Holarctic ranges for T. krabbei and T. hydatigena are likely constrained
by the temporal limits for expansion into Beringia and North America by
an assemblage involving wolves and primary ruminant (cervid) interme-
diate hosts (Rausch, 1994). Sympatry for constituents of this host assem-
blage probably extends to 2Ma in North America (Guthrie and Matthews,
1971) such that these cestodes could have become broadly established
prior to or early in the Pleistocene. The history is obscured by the unre-
solved status for T. krabbei and the recognition of multiple cryptic spe-
cies that may be widely distributed at high latitudes in canids and ursids
(Lavikainen et al., 2010, 2011). At high latitudes in the absence of wolves,
Arctic fox serve as primary definitive hosts for T. krabbei.
Ursids had not been considered as hosts for characteristic taeniids or
other cyclophyllidean tapeworms (Abuladze, 1964; Rausch, 1994). Reports
of infections by Taenia were generally limited to species such as T. krabbei or
T. hydatigena that typically circulate between canid definitive and ungulate
intermediate hosts. A putative cryptic species, similar to T. krabbei, was ini-
tially demonstrated based on sequence data from mitochondrial DNA for
cysticerci in moose (Alces alces) from Fennoscandia (Lavikainen et al., 2010).
Recently described as T. arctos, it has been shown to circulate in brown
bear (U. arctos) from both Fennoscandia and Alaska (Haukisalmi et  al.,
2011; Lavikainen et al., 2011). Brown bears and moose (Alces americanus)
are relatively late immigrants across Beringia into the Nearctic during the
ultimate Wisconsinan glaciation (Kurtén and Anderson, 1980), and this
expansion may account for the apparent Holarctic distribution of this
­species of Taenia. Such a distribution is consistent with radiation for Taenia
among Eurasian carnivorans prior to expansion into North America. The
occurrence of T. arctos in black bears or polar bears is unknown.
Current evidence suggests that only taeniids in mustelids show strong
evidence of associations linked to cospeciation. More generally, it appears
Northern Host–Parasite Assemblages     31

that geographic colonisation and guild dynamics related to common prey

species for canids, felids, hyaenids and ursids account for parasite diversi-
fication and distribution among assemblages of large carnivores (Hoberg,
2006). Taenia would have had a complex history in northern environ-
ments due to extensive levels of sympatry and episodes of synchronicity
among a diverse assemblage of carnivorans in the Pliocene and Pleisto-
cene (Guthrie, 1968a). Host switching among carnivorans within guilds
has been postulated as a primary mode for diversification among these
tapeworms where patterns of diversity may be related to the relative size
spectrum and foraging behaviour of definitive hosts. For example, arrays
of closely related species circulate through rodent intermediate hosts and
occur in mustelids, small canids and felids; similar relationships are also
apparent for transmission through ungulates including moose and cari-
bou for species of Taenia that occur in megacarnivores such as wolf, bear
and large cats (Hoberg, 2006; Haukisalmi et al., 2011). Echinococcus spp. among canids

At high latitudes, there are two species of the taeniid Echinococcus that,
respectively, circulate in obligate predator–prey cycles among small
canids and arvicoline rodents (E. multilocularis) and among wolves (and
dogs) and ungulates including moose and caribou (tentatively, the cer-
vid strain of E. granulosus, G-8, or E. canadensis) (Rausch, 1967; Thompson
et al., 2005; Nakao et al., 2007).
The distribution of E. multilocularis reflects the intricate history of
V. vulpes in North America, although V. lagopus may have had an over-
riding role in distribution, particularly at high latitudes in the circumpo-
lar zone. Based on analyses of mitochondrial loci, recognised northern
Eurasian and North American partitions for E. multilocularis appear to
reflect distributions dating to the ultimate Sangamon interglacial, coincid-
ing with eastward expansion across Beringia during the Illinoian glacial
stage (Nakao et  al., 2009). Secondarily, populations were isolated north
and south of the Laurentide with E. multilocularis persisting in Arctic fox
(St Lawrence Island samples and N1 haplotype) and possibly in the
eastern subclade of red fox during the Wisconsinan glacial maximum
(N2 haplotype); red foxes representing this early colonisation of North
America became extinct in Beringia and were later replaced by those of
Eurasian origin in the Wisconsinan. Shallower histories for populations
of E. multilocularis found in Eurasia and the amphiberingian region may
be linked to this later expansion and to the continuity of red fox across
the Palaearctic and a subsequent invasion of Beringia (A2 and A4 hap-
lotypes) (see Nakao et  al., 2009). Such a history in the Beringian region
modifies the current narrative and would account for the distribution of
parasite haplotypes including endemic Alaskan and Asiatic populations
32     Eric P. Hoberg et al.

on St ­Lawrence Island, Alaska (Nakao et al., 2009). Such is also concordant

with the history for both Arctic fox and red fox, but corroboration requires
more comprehensive sampling across the range of E. multilocularis.
In North America, post-Pleistocene expansion to the north and west
from southern refugia involving an initial small population of parasites in
red fox may account for the apparent genetic uniformity for these cestodes
in temperate North America, although this region has yet to be adequately
sampled (Nakao et  al., 2009). These populations of red fox, however,
appear to be beyond the historical limits of the endemic eastern subclade
(Aubry et al., 2009) and may also reflect interactions with introduced foxes
imported during the 1800s (Rausch, 1994). Genetic uniformity also does not
exclude the hypothesis for a recent introduction of E. multilocularis estab-
lishing the central North American focus with subsequent and ongoing
geographic expansion over the past few hundred years (Rausch, 1985). In
contrast, southward postglacial expansion of red fox out of eastern Berin-
gia into Yukon Territory and British Columbia may have been blocked by
taiga forest habitats, where the parasite apparently does not occur (Rausch,
1967). The history and biogeography for E. multilocularis would be expected
to parallel that of T. crassiceps and T. polyacantha that circulate among foxes
and arvicoline rodent intermediates (Rausch, 1994). Interestingly, a recent
discovery of E. multilocularis in British Columbia, representing the west
central European population, indicates a very recent introduction and
establishment of this taeniid in contemporary time by jump dispersal and
appears to be unrelated to deeper historical processes (Jenkins et al., 2012).
Arctic fox, however, may be most critical as a determinant of high-
latitude distributions. Consequently, there may be different expectations
for population structure in E. multilocularis associated with red fox in
contrast to Arctic fox. The latter would be predicted to show signatures
of extensive gene flow across the broad geographic range where arvico-
lines are present (Rausch, 1994). Complex historical interactions involving
temporal shifts or episodes of sympatry for foxes and arvicoline rodents
including species of Microtus, Myodes and Lemmus have determined the
distribution of the parasite in space and time. Voles may be the limiting
factor in determining local occurrence and transmission (e.g. Henttonen
et al., 2001), but definitive hosts with varying levels of vagility and dif-
ferential responses to glacial maxima would either mediate isolation (red
fox) or gene flow (Arctic fox).
Recurrent expansion in conjunction with high mobility may confound
recognition of the history for E. granulosus (genotypes G-8 and G-10)
(Lavikainen et  al., 2003; Thompson et  al., 2005) and the assemblage of
carnivores (primarily wolf) and cervids that perpetuate transmission in
northern environments. Genetic sampling has thus far been insufficient
to either document the geographic range or the host associations and
identity for Echinococcus circulating among wolves, caribou, moose and
Northern Host–Parasite Assemblages     33

related cervids or infer the relationship for populations across the Arctic
and extending to temperate latitudes in North America and Eurasia. Diphyllobothrium spp

Among the approximately 50 recognised species of Diphyllobothrium,
relatively few are known to occur at high latitudes (Scholz et  al., 2009).
Considering Alaska and the Canadian Arctic, six species (D. alascense,
D. dalliae, D. dendriticum, D. lanceolatum, D. latum and D. ursi) are likely
to circulate among terrestrial carnivores and all except D. alascense also
occur in people (Rausch et al., 1967; Rausch and Hilliard, 1970). Although
a detailed phylogeny for Diphyllobothrium has yet to be developed, it is
likely that most of these species had extended histories at high latitudes
during the Pleistocene. As a potentially zoonotic assemblage, diphyllo-
bothriids have been associated with people coincidental with the earli-
est incursions out of Eurasia into North America and in conjunction with
diets rich in both freshwater and anadromous fishes that serve as inter-
mediate and paratenic hosts (e.g. Rausch et al., 1967; Rausch and Hilliard,
1970; Scholz et al., 2009). Diphyllobothrium latum, however, appears to be
primarily a parasite of people and its historical occurrence at high lati-
tudes may reflect both late Pleistocene expansion across Beringia and later
anthropogenic introductions with Europeans establishing focal distribu-
tions in the eighteenth century (Rausch and Hilliard, 1970).
At northern latitudes, particular species of Diphyllobothrium in terres-
trial carnivores circulate in freshwater (D. latum, D. dalliae, D. dendriticum),
marine (D. alascense, D. lanceolatum) or freshwater/marine cycles (D. ursi).
Additional species, including D. pacificum, D. stemmacephalum, D. fayi, D.
hians and D. cordatum are characteristic of marine mammals (either pinni-
peds or cetaceans) and potentially may be available in terrestrial systems
through anadromous fishes or exploitation of marine fishes in estuarine
environments (Rausch and Adams, 2000; Rausch, 2005; Scholz et al., 2009;
Rausch et al., 2010). Diphyllobothrium and related diphyllobothriids (e.g.
Diplogonoporus, Pyramicocephalus) appear to have a long and complex his-
tory with arctoid carnivorans and cetaceans, in part involving Beringia
and the Arctic basin with connections through Bering Strait minimally
over the past 4–5 Myr (Hoberg and Adams, 2000). Resolution of this his-
tory and connections to the global fauna remains obscured by the absence
of comprehensive phylogenetic studies among this group of cestodes. Other helminths among carnivorans

Other helminth taxa, including an assemblage of nematodes, are well rep-
resented among carnivorans in the circumpolar region, and it is apparent
that some components of these faunas have histories of expansion across
Beringia from Eurasia during the Pleistocene (e.g. Rausch et  al., 1979).
34     Eric P. Hoberg et al.

Host distributions in most cases also suggest deep associations and early
diversification with feliforms and caniforms, and some level of host col-
onisation is also postulated where single species may be shared among
ecologically similar carnivores. Comprehensive and detailed phylogenetic
studies are lacking, however, and robust hypotheses for host association
and biogeography remain to be defined. Examples include the ascarids
Baylisascaris, with species distributed among mustelids, mephitids, ursids
and felids, or Toxascaris occurring among canids, ursids and felids. Among
the strongyles, species of Molineus (Molenioidea) also have Holarctic dis-
tributions and broad associations among multiple carnivoran groups.
Considering other strongyles, hookworms (Ancylostomatoidea) includ-
ing species of Uncinaria in ursid hosts have been explored to some degree in
the amphiberingian region (Rausch et al., 1979). Three species (U. rauschi,
Nearctic; U. yukonensis, Holarctic, and U. skrjabini, Palaearctic) are currently
recognised in brown bears and black bears (Wolfgang, 1956; Olsen, 1968).
It is postulated that U. yukonensis originated in eastern Eurasia, expanded
with U. arctos across Beringia in the late Pleistocene and secondarily colo-
nised U. americanus in North America during the Holocene (Rausch et al.,
1979). It is possible that U. rauschi represents an earlier event of geographic
colonisation by bears and hookworms into North America from Eurasia.
Uncinaria skrjabini may actually be a characteristic parasite in some muste-
lids and its occurrence in ursine hosts may be attributable to colonisation
(Kontrimavichus, 1969). It is apparent that species assemblages of para-
sites circulate among diverse arrays of carnivoran hosts as exemplified by
studies of faunal structure for parasites of black bears from North America
or circumpolar mustelids (e.g. Kontrimavichus, 1969; Pence et  al., 1983;
­Koehler et al., 2007).

1.4.2. Faunas associated with Lagomorpha

• The parasite groups: Cestoda – Cyclophyllidea, Anoplocephalidae
(Mosgovoiya, Schizorchis); Nematoda – Strongylida, Trichostrongylina
(Heligmosomoidea – Ohbayashinema; Molineoidea – Murielus, Graphi-
diella, Rauschia; Trichostrongyloidea – Obeliscoides); Metastrongylina
(Protostrongylus). Oxyuroidea, Heteroxynematidae (Cephaluris, Labios-
tomum). Taxonomy is consistent with Boev (1975); Durette-Desset et al.
(1994); Anderson (2001) and Chilton et al. (2006) (Table 1.5).
• The host groups: Lagomorpha – Ochotonidae (Ochotona spp.); Lepori-
dae (Lepus spp.)
• Taxonomy for lagomorphs consistent with Wilson and Reeder (2005).
Lagomorphs, Leporidae and Ochotonidae diversified initially in Eurasia
during the Oligocene and later attained Holarctic distributions estab-
lished across Beringia during the late Tertiary (Dawson, 1967); no species
in these groups have Holarctic ranges. A number of apparent sister groups
Northern Host–Parasite Assemblages     35

among the helminths (e.g. Anoplocephalidae – Schizorchis and Mosgovoiya;

Trichostrongylina – Murielus, Rauschia + Nematodiroides; Oxyuroidea –
Dermatoxys, Cephaluris and Labiostomum) indicate deep coevolutionary
associations for assemblages of parasites in Leporidae and Ochotonidae
(e.g. Gvozdev, et al., 1970; Quentin, 1975).
Pikas include 30 extant species, but only Ochotona collaris and O. princeps
occur in the Nearctic and represent initial expansion into North America
during the late Pliocene (Smith et al., 1990; Yu et al., 2000). Transcontinental
distributions for Trichostrongylina (Ohbayashinema, Murielus, Graphidiella),
Oxyuroidea (Labiostomum and Cephaluris) and Anoplocephalidae (Schizor-
chis) involving phylogenetically diverse and divergent species of Ochotona
are consistent with a deep history of association linking localities in the
Palaearctic and Nearctic over the late Tertiary and Pleistocene (Galbreath,
2009; Galbreath and Hoberg, 2012; Durette-Desset et  al., 2010). The his-
tory of these parasite taxa is complex and intricate with most representing
strongly host-specific helminths limited to Ochotona (Gvozdev, 1962; See-
see, 1973). For example, Ohbayashinema appears associated with an early
event of host colonisation in Eurasia following the divergence of Lepori-
dae and Ochotonidae; these nematodes have affinities with Citellinema in
sciurids or Heligmosomoides in arvicolines (Durette-Desset et al., 2010). In
contrast, both Murielus and Schizorchis appear to have deeper coevolution-
ary histories with patterns of divergence linked to the common ancestor
for the Leporidae + Ochotonidae (Rausch, 1994; Hoberg 2005a).
The helminth fauna of pikas was initially assembled in Eurasia from
phylogenetically disparate sources over an extended time frame since
the mid Tertiary. Geographic expansion from Eurasia and colonisation
across Beringia and south into the Nearctic occurred under the influence
of episodic climate change and cyclical habitat modification during the
past 2Myr (Hoberg, 2005a; Galbreath, 2009). Refugial habitats in North
America were important in the maintenance of complex parasite assem-
blages and in the generation of considerable cryptic diversity across most
parasite groups (Galbreath, 2009; Galbreath and Hoberg, 2012).
Although the helminth fauna characteristic of pikas is relatively
diverse (e.g. Rausch, 1994; Hoberg, 2005a; Hoberg et al., 2009; Galbreath,
2009; Durette-Desset et al., 2010; Galbreath and Hoberg, 2012), few para-
site taxa are distributed at higher latitudes, particularly in the Nearctic.
Comparisons of the sister species O. collaris (Subarctic) and O. princeps
(Temperate) in western North America indicate the complete absence of
trichostrongyline nematodes at higher latitudes in the former host (Gal-
breath, 2009; Galbreath and Hoberg, 2012). Further, there are no unique
species of pinworms and only one endemic cestode at higher latitudes
such that the fauna mostly represents a subset of the parasite species that
are characteristic of the southern O. princeps. Following the initial estab-
lishment of pikas in North America, these small lagomorphs became
Eric P. Hoberg et al.
TABLE 1.5  Species diversity and biogeography for exemplar helminth parasites among Lagomorpha in the Arctic and Subarctic, exploring
assemblages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected for
global diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic

Parasite taxon Host association Distribution Species diversitya Processesb

Schizorchis spp.c Ochotonidae Holarctic/disjunct (10+G/0H/5N/5P) (2, east GE, R
and west Beringia)
Mosgovoyia Leporidae Holarctic/disjunct (5G/2H/1N/2P) GE
Murielus spp. Ochotonidae Holarctic/disjunct (3G/0H/1N/2P) GE
(absent from Beringia)
Obeliscoides Leporidae Holarctic (3G/0H/1N/2P) GE
Graphidiella spp. Ochotonidae Holarctic/disjunct (4G/0H/1N/3P) GE
(absent from Beringia)
Ohbayashinema spp. Ochotonidae Holarctic/disjunct (6G/0H/2N/4P) GE, R
(absent from Beringia)
Rauschia spp. Leporidae Holarctic/disjunct (5G/0H/2N/3P) GE
(absent from Beringia)
Trichostrongylus spp.d Bovidae/Cervidae, Holarctic (30+G/0H/7N/23P) GE, HC
Leporidae, Rodentia
Protostrongylus spp. Leporidae Holarctic (6G/1H/1N/4P) GE
Cephaluris spp. Ochotonidae Holarctic – disjunct (10+G/1H/3N/6P) GE, R
Labiostomum (Eugenuris) Ochotonidae Holarctic – disjunct (10+G/0H/4N/6P) GE, R
Labiostomum (Labiostomum) Ochotonidae Holarctic – disjunct (7+G/0H/3N/4P) GE, R
a  Species diversity relative to regions: G = global, H = Holarctic, N = Nearctic, P = Palaearctic.
b  Processes include geographic expansion = GE; host colonisation = HC; refugial effects = R.
c  Diversity includes undescribed species (Hoberg et al., 2009; Galbreath and Hoberg, 2012).

d  Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

Northern Host–Parasite Assemblages    

38     Eric P. Hoberg et al.

extinct in Beringia but were continuous in habitats south of the Lauren-

tide. Subsequent expansion from southern refugia (leading to the origin
of O. collaris) along with local extinction for the trichostrongylines are
implicated as major influences on patterns of current diversity in the Sub-
arctic (Galbreath, 2009; Galbreath and Hoberg, 2012). Thus, parasites tell
us a story that is counter to the usual narrative for Beringian biogeogra-
phy, indicating a greater role for dispersal from temperate North America
into Beringia prior to the terminal Wisconsinan as a driver for diversity in
northern systems.
Considering Leporidae, four species of hare occur at high latitudes
across the Holarctic and include Lepus timidus (snow hare – Palaearctic),
Lepus othus (Alaska hare – western Alaska), L. arcticus (Arctic hare, north-
eastern Arctic Canada and Greenland) and L. americanus (snowshoe hare
– widespread in Subarctic to Arctic North America) (MacDonald and
Cook, 2009; Waltari and Cook, 2005). An Arctic clade of leporids includes
L. townsendii (white-tailed jackrabbit of western temperate North Amer-
ica) with L. othus, L. arcticus and L. timidus (Halanych et al., 1999). Lepus
americanus is sister of a western American clade of Lepus (Halanych et al.,
1999) and is infected with Protostrongylus boughtoni, Obeliscoides cuniculi
and species of Rauschia probably throughout the geographic range occu-
pied in North America. None of these parasites is known in the Alaska
hare or Arctic hare that are parapatric with L. americanus in some parts of
its range (MacDonald and Cook, 2009). Another lungworm, Protostrongy-
lus cf. pulmonalis, occurs in some populations of Alaska hare and also in
Lepus townsendi (white-tailed jackrabbit) at temperate latitudes of west-
ern North America but is absent in L. americanus (Boev, 1975; E.P. Hoberg
and E. Waltari, unpublished data). Protostrongylus pulmonalis has a broad
host and geographic range in the Palaearctic but, in North America, is
represented by disjunct and putatively discrete populations north and
south of the former Laurentide glaciation suggesting a complex pattern
of refugial isolation and parasite extinction (E.P. Hoberg and E. Waltari,
unpublished data).
Obeliscoides, Protostrongylus, and Rauschia appear to have ancestral
ranges in the Palaearctic including L. timidus and other Eurasian lepo-
rids. Current host and geographic associations suggest multiple events
of expansion between Eurasia and North America, although direction-
ality remains equivocal (Waltari and Cook, 2005); secondarily, isola-
tion occurred north and south of continental glaciers in the Nearctic
for this fauna in leporids. Absence of lungworms and other strongyles
in L. arcticus appears consistent with loss of parasites in a high Arctic
refugium for hosts during the terminal glacial stages of the Pleistocene
(Waltari and Cook, 2005). Similar to the pattern of parasite diver-
sity in O. collaris, the reduced fauna may reflect limitations imposed
by extreme environments and/or demographic and founder effects
Northern Host–Parasite Assemblages     39

involving small initial host populations and geographic colonisation

on the periphery of northern ranges.

1.4.3. Faunas associated with Rodentia

• The parasite groups: Cestoda – Cyclophyllidea, Anoplocephalidae
(Anoplocephaloides, Diandrya, Macrocephaloides, Marmotocephala (=Sciuro-
taenia), Paranoplocephala, Paranoplocephaloides, Parasciurotaenia); Hyme-
nolepididae (Arostrilepis); Nematoda – Strongylida, Trichostrongylina,
Heligmosomoidea – (Citellinema, Heligmosomoides, Heligmosomum);
Oxyuroidea (Citellina). Taxonomy is consistent with Durette-Desset
et  al. (1994), Anderson (2001), Chilton et  al. (2006) and Haukisalmi
(2009) (Table 1.6).
• The host groups: Rodentia – Cricetidae, Arvicolinae (Dicrostonyx, Lemmus,
Myodes, Microtus, Phenacomys, Synaptomys), and Neotominae (Pero-
myscus); Sciuridae, Sciurini (Tamiasciurus), and Marmotini (Marmota,
Spermophilus). Taxonomy is consistent with Wilson and Reeder (2005).
Rodents are the most diverse group of mammals and occur globally in a
variety of ecosystems, although many genera and species exhibit specific
habitat associations. As a consequence, these small mammals are critical
indicators of environmental structure in evolutionary and ecological time
(e.g. Hoffmann, 1981; Repenning, 2001). Although the earliest rodents
appear in the Palaeocene (65–55Ma) of North America, the structure of
contemporary faunas has largely been determined since the mid Tertiary
and has been strongly influenced by expansion events from Eurasia
into the Nearctic that continued through the Quaternary. The primary
Holarctic and North American taxa are represented by Cricetidae (130
genera and 681 species notably including Arvicolinae and Neotominae)
and Sciuridae (51 genera and 278 species notably including Sciurinae
and Marmotini) (Musser and Carleton, 2005; Thorington and Hoffmann,
2005). In our discussion, we focus on a limited number of exemplars
among the rodents where both host and parasite biogeographic history
has been examined.
Rodent helminth faunas have been explored in considerable detail
across higher latitudes of the Holarctic (e.g. Rausch, 1952, 1957; Durette-
Desset, 1968, 1971; Durette-Desset et al., 1972; Rausch and Rausch, 1973;
Ryzhikov et al., 1978, 1979). Faunas exhibit complex patterns of geographic
and host colonisation and regional extinction with limited evidence of
diversification through extensive cospeciation (Haukisalmi et  al., 2008).
Holarctic distributions are linked to dispersal events across Beringia from
the Pliocene into the Quaternary (Rausch, 1994).
Cricetid rodents have a long history of connections between Eurasia and
the Nearctic. Among these, the Arvicolinae and their helminths are among
the most informative exemplars for revealing historical patterns and
TABLE 1.6  Species diversity and biogeography for exemplar helminth parasites among Rodentia in the Arctic and Subarctic, exploring assem-
blages influenced by episodic climate change and geographic expansion in the Pliocene and Quaternary. Species richness is reflected for global

Eric P. Hoberg et al.

diversity, distributions across the Holarctic and those that are endemic to either the Nearctic or the Palaearctic

Parasite taxon Host association Distribution Species diversitya Processesb

Arostrilepis spp.c Arvicolinae Holarctic/Beringian (13G/2H/4N/7P) GE, HC, R
(+Geomyidae) (5 amphiberingian)
Anoplocephaloides spp.c Arvicolinae Holarctic/Beringian (10G/2H/3N/3P) GE, HC, R
(3 amphiberingian)
Diandrya Sciurinae Nearctic/Beringian (1N) GE, HC
Paranoplocephala spp. Arvicolinae (+Sciurinae) Holarctic/Beringian (35G/8H/13N/14P) GE, HC, R
(15 amphiberingian)
Paranoplocephaloides spp. Arvicolinae Holarctic (2G/0H/1N/1P) GE
Parasciurotaenia Sciurinae Palaearctic (1G/0H/0N/1P) HC
Marmotocephala spp. Sciurinae Holarctic/Beringian (2G/1H/0N/1P) HC
(1 amphiberingian)
Microcephaloides spp.c Arvicolinae Holarctic/Beringian (9G/0H/6N/3P) GE, HC, R
Catenotaenia spp. Muridae, Cricetidae, Holarctic/Beringian (22+G/2H?/5N12P) GE, HC
Arvicolinae, Mamotinae
Citellinema spp. Sciuridae Holarctic (10+G/0H/5N/5P) GE
Heligmosomoides spp.d Arvicolinae Holarctic/Beringian (36+G/1H/17N/19P) GE, HC, R
(other Cricetidae
Trichostrongylus spp.e Bovidae/Cervidae Lepori- Holarctic (30+G/0H/7N/23P) GE, HC
dae, Rodentia
Citellina spp. Sciuridae Holarctic (11+G/0H/2N/9P) GE, HC
a  Species diversity relative to regions: G = global, H = Holarctic, N = Nearctic, P = Palaearctic.
b  Processes include geographic expansion = GE; host colonisation = HC; refugial effects = R.
c  Species richness for Arostrilepis, Anoplocephaloides and Microcephaloides includes undescribed diversity in each genus.

d  Heligmosomoides includes nominal species and subspecies (see Asakawa, 1988).

e  Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

Northern Host–Parasite Assemblages    

42     Eric P. Hoberg et al.

processes of dispersal and diversification. Over the Pliocene and Pleis-

tocene, 16 arvicoline genera encompassing 5 distinct faunas have been
involved in expansion, primarily asymmetrical, from Eurasia into North
America ­(Conroy and Cook, 1999; Repenning, 2001). Episodes for expan-
sion and isolation correlate with cyclical periods of glaciations; the first
North American glacial episode occurred around 2.65Ma (Pliocene),
and the first of the classical sequences (Nebraskan) is calibrated near
650–850Ka. Multiple events for geocolonisation from Eurasia are brack-
eted by these time frames and later into the Pleistocene: (1) bog lemmings,
Synaptomys (=Mictomys) at 2.65Ma; (2) Phenacomys at 2.5Ma; (3) Microtus at
2.5Ma in Beringia (1.7Ma south of Laurentide) and later at 300Ka; (4) the
ancestor for Lemmus is known about 2.5Ma in west and east Beringia; Lem-
mus and Dicrostonyx are known since about 1Ma in Beringia from Eurasia,
and for these lemmings, contemporary ranges do not extend to regions
south of the former Cordilleran and Laurentide glaciations, although
southern refugial distributions are postulated (Guthrie, 1968b; Guthrie
and ­Matthews, 1971; Repenning, 2001; Fedorov and Goropahsnaya, 1999;
­Fedorov et al., 1999, 2003; Fedorov and Stenseth, 2002), and (5) Red-backed
voles ­(Myodes) are recognised near 850Ka in Beringia (Repenning, 2001).
It is evident that distinct faunas were partitioned in space and time over
the past 5Ma, influenced by dispersal events (inter- and ­intracontinental)
strongly correlated with specific climatological episodes (Conroy and
Cook, 1999, 2000; Repenning, 2001).
A complex biogeographic history also coincided with a rapid radiation
for voles and lemmings across circumpolar habitats (Conroy and Cook,
1999, 2000; Repenning, 2001; Cook et al., 2004; Galbreath and Cook, 2004).
Most palaeolineages retain extant descendants, although relatively few
genera and species are now found at Subarctic to Arctic latitudes (e.g. in
the contemporary fauna, 53% are strictly temperate, 33% temperate to
Subarctic and 13% Arctic) (Repenning, 2001). These observations have
suggested that dispersal events for rodents on intercontinental scales coin-
cided with temperate climates (or habitats) in Beringia. The corollary is
that faunal structure evident in contemporary systems resulted from an
exchange of temperate faunas that are now absent in Beringia but with
distributions now extending into more southern latitudes in both Eurasia
and North America (Repenning, 2001). Although multiple genera are Hol-
arctic in distribution, most of these taxa have disjunct ranges with large
gaps at high latitudes. Only three species of arvicolines, Myodes rutilus,
Microtus oeconomus and Lemmus sibiricus, have continuous distributions
that span Beringia (Rausch, 1994). These distributions and their interpreta-
tion represent part of the apparent habitat paradox (i.e. at what point were
temperate habitats continuous across the land bridge?) for Beringia during
glacial stages. Habitat structure is critical either in impeding or in facilitat-
ing intercontinental expansion and may have significance for the question
Northern Host–Parasite Assemblages     43

of whether greater Beringia was primarily a continuous steppe at higher

latitudes or a complex mosaic of xeric and mesic microhabitats (Guthrie,
2001; Elias and Crocker, 2008). It is apparent that these heterogeneous
environments linking Eurasia and North America were intermittently
of high productivity and capable of supporting a diverse assemblage of
mammals (Guthrie, 1982, 1984, 1990, 2001; Repenning, 2001).
Phylogeographic breaks observed across the Kolyma uplands near the
western boundary of Beringia for multiple arvicoline host taxa (Microtus
oeconomus, Lemmus spp., Dicrostonyx spp.) possibly correspond to his-
torical barriers due to past (intermittent) glaciations reinforced by habitat
structure during interglacials (e.g. xeric environments as ecological barri-
ers) (Galbreath and Cook, 2004). These relationships point to both glacial
(ice masses) and interglacial (habitat refugia) drivers that have influenced
isolation and diversification for arvicoline hosts (Conroy and Cook, 2000;
Repenning, 2001). Thus, among rodents, apparently it is expansions of
Subarctic to temperate habitats (not arctic habitat) that has facilitated the
majority of intercontinental faunal exchange. This association seems also
to apply to large ungulates associated with Beringian and periglacial habi-
tats of the Pleistocene (Guthrie, 2001).
In contrast to cricetids, the sciurid rodents have a substantially deeper
history across the Northern Hemisphere with apparent origins in the
Nearctic prior to expansion and radiation in Eurasia (Kurtén and Ander-
son, 1980). The divergence of ground squirrels (Spermophilus with 38 spe-
cies total/25 North American/1 Holarctic) and marmots (Marmota with 14
species/6 North American) is estimated near 9–10Ma and a complex his-
tory across Beringia is evident (Steppan et al., 1999; Galbreath et al., 2011).
Overall the structure of contemporary diversity among rodents repre-
sents a process of dynamic faunal assembly over time, reflecting the inter-
play between persistence and turnover (Repenning, 2001). Distributions
for various taxa resulted from complex interactions between climatic oscil-
lations (e.g. glacial/interglacial and stadial/interstadial cycles that influ-
enced habitat, and pathways for expansion) and life history parameters
(e.g. vagility and persistence in evolutionary and ecological time). Under
this model, tundra-adapted (Arctic) faunas that have persisted within
Beringia throughout the Quaternary are represented by the lemmings,
Dicrostonyx and Lemmus (Fedorov and Goropahsnaya, 1999; Fedorov et al.,
1999, 2003). These contrast with transient faunas moving through Beringia
as they track temporal shifts in suitable habitat. Such movements have
resulted in Boreal/Subarctic disjunct distributions exemplified by spe-
cies of Myodes and Microtus (Repenning, 2001). This mosaic of persistent
and transient rodent assemblages has in turn been an important driver for
parasite faunal structure.
Cestode faunas in northern rodents are dominated by two fami-
lies, Anoplocephalidae and Hymenolepididae (Taeniidae that occur as
44     Eric P. Hoberg et al.

­ etacestodes are excluded here). Collectively these taxa represent the most
diverse helminth groups among any of the terrestrial mammals at high
latitudes with distributions extending south into the Nearctic and Eurasia.
This may reflect host group diversity for cricetids (Arvicolinae with 28 gen-
era and 151 species) and sciurids (Marmotini with 6 genera and 92 species),
although a disproportionate representation of cestodes is apparent at higher
latitudes particularly among arvicolines. Histories for these respective ces-
tode groups among arvicolines are postulated to represent independent
radiations following single basal colonisation events from Lagomorpha for
anoplocephalines and from Soricomorpha for the hymenolepidid Arostril-
epis in the Palaearctic (Wickström et al., 2005; Haukisalmi et al., 2010).
Among the anoplocephalines, diversity is manifested by a relatively
large number of related genera (7) and species (estimated + 60) partitioned
primarily among Holarctic cricetids (Arvicolinae/voles and lemmings)
and sciurids (Marmotini/marmots and ground squirrels) and some
Nearctic geomyids (pocket gophers) (Gvozdev et  al., 2004; Haukisalmi
et  al., 2002, 2004; Wickström et  al., 2005; Haukisalmi et  al., 2006, 2008,
2009; Haukisalmi, 2009). Further, in this assemblage multiple cryptic spe-
cies have been demonstrated within A. dentata (4 spp.), Microcephaloides
variabilis (6), Paranoplocephala omphalodes (4) and possibly P. macrocephala
(Haukisalmi et  al., 2004, 2008, 2009). Species of Paranoplocephala are pri-
marily parasites of Microtus voles, with relatively fewer species occur-
ring among lemmings or the red-backed voles (Wickström et  al., 2003;
Haukisalmi et al., 2006).
Phylogenetic relationships among species of Paranoplocephala, Anoplo-
cephaloides, Microcephaloides and other genera remain enigmatic, but avail-
able evidence suggests a period of explosive radiation leading to multiple
parasite lineages coinciding with events for host diversification extend-
ing into the Pliocene (Conroy and Cook, 1999, 2000; Cook et  al., 2005;
Haukisalmi et  al., 2006). A single colonisation event is evident among
early arvicolines, but arvicolines have served as a source for colonisation
and subsequent diversification of cestodes among other rodent groups
(Haukisalmi et  al., 2004; Haukisalmi, 2009). In the Nearctic, these have
included parasites of geomyids (Microcephaloides and Paranoplocephala),
marmots (Diandrya and Marmotocephala) and other sciurids (some species
of Paranoplocephala). Interestingly, Diandrya composita resulted from colo-
nisation of Nearctic marmots from arvicolines, probably Dicrostonyx lem-
mings during the Pleistocene (Wickström et al., 2005). The cestode faunas
of Eurasian and Nearctic marmots are distinct with no genera or species
that are shared (Rausch, 1994).
Rausch (1994) reviewed the status of helminth faunas of large rodents
in the Beringian region and described a history of expansion between
the Palaearctic and Nearctic. In contrast to arvicolines, helminth diver-
sity is minimal in sciurids and few cestodes are considered typical or are
Northern Host–Parasite Assemblages     45

­widespread (Ryzhikov et al., 1978, 1979). Among cestodes, these include

the anoplocephalids Parasciurotaenia, and Ctenotaenia and the catenotaeniid
Catenotaenia primarily in Eurasia, Marmotocephala with a limited Eurasian–
Beringian range and Diandrya in the Nearctic. Nematode faunas are
dominated by spirurids such as Rictularia and Mastophorus and oxyurids
represented by Citellina and Syphacia. The historical biogeography of these
groups has not been examined in detail. Parasites may be particularly rare
among arboreal sciurids in contrast to marmots and ground squirrels.
Pervasive patterns of host and geographic colonisation and rapid
generic- and species-level diversification characterise the history of the
arvicoline clade of anoplocephaline cestodes (Wickström et al., 2001, 2003;
Haukisalmi et al., 2004; Wickström et al., 2005). These shifts were played
out against climatic oscillations and episodes of environmental perturba-
tion during the late Pliocene and Pleistocene, factors considered as criti-
cal drivers for diversification in complex host–parasite assemblages (e.g.
Hoberg and Brooks, 2008, 2010).
In contrast, hymenolepidids are represented by the genus Arostrilepis
where there are now 13+ recognised species-level lineages within what had
historically been recognised as A. horrida, a single widespread and morpho-
logically variable species (Hoberg et al., 2003; Cook et al., 2005; Makarikov,
2008; Makarikov and Kontrimavichus, 2011; Makarikov et al., 2011, in press;
K.E. Galbreath and E.P. Hoberg, unpublished data). Among these, seven are
limited to the Palaearctic, two are Beringian/Holarctic and four are endemic
to the Nearctic. The limits for diversity and species richness for Arostrilepis
remain to be clearly defined and, for example, may include additional spe-
cies in arvicolines (Myodes andersoni and M. smithii) from Japan (Asakawa
et  al., 2002). These distributions and apparent host associations reflect a
deep history with arvicolines extending into the Pliocene of Eurasia. Such
is indicated by conspecificity of Arostrilepis in Lemmus and Synaptomys, the
occurrence of an endemic species in Myodes gapperi and multiple species par-
titioned between Microtus spp. and Myodes spp. in the Nearctic and eastern
Palaearctic (Cook et al., 2005); multiple expansion events from the Palaearc-
tic are evident for both hosts and parasites. For example, an initial colonisa-
tion of North America is indicated for the precursor of M. gapperi in the late
Pliocene/early Pleistocene, whereas the distribution of the Holarctic M. ruti-
lus was established during Wisconsinan time of the late Pleistocene (Cook
et al., 2004). Further, three species of tapeworms, respectively, in Geomyidae
(pocket gophers, Thomomys), Neotominae (deer mice, Peromyscus) and Sciu-
ridae (Tamiasciurus) indicate a role for host colonisation from arvicolines in
diversification of Arostrilepis in North America (Makarikov et al., in press).
Cestode faunas among arvicolines have responded to micro-refugial
events (Anoplocephaloides spp., Microcephaloides spp. and Paranoplocephala
spp.) and larger scale patterns of regional isolation (Arostrilepis spp.).
Striking differences in faunal diversity (generic and species richness)
46     Eric P. Hoberg et al.

may be attributable to life history, patterns of abundance and dispersion

(homogeneous vs. discontinuous or patchy distributions geographically
and within hosts at specific localities) and effective population size
(Hoberg et al., 2003; Cook et al., 2005). This contrast in diversity is notable,
however, given the apparent equivalent age of association for these dispa-
rate cestode groups in rodents.
Several explanations may be explored for divergent patterns of diver-
sity among these tapeworm assemblages. For example, are there differences
in historical centres and the timing of diversification for anoplocephalines
and Arostrilepis? (1) Did Arostrilepis initially radiate in central Eurasia and
secondarily expand across Beringia into the Nearctic? (2) Did diversifi-
cation for Anoplocephaloides, Paranoplocephala and related genera initially
occur through regional isolation and secondarily by local geographic iso-
lation on near landscape scales? (3) How have faunas been influenced by
single or multiple events for expansion, establishment and isolation at
intercontinental, intracontinental and landscape scales? (4) Sciurids are
older but helminth diversity is generally lower than that seen in arvico-
lines; does this pattern reflect the role of timing for host colonisation in fau-
nal assembly (e.g. late in the evolution of marmots or ground squirrels)?
Life history also contributes to differences in cestode diversity. Species
of anoplocephalines are not regionally widespread; although occasionally
locally abundant, distributions are generally heterogeneous and patch-
ily distributed with few individual worms within hosts and few infected
voles (or lemmings) at local scales (Haukisalmi et  al., 2008). These fac-
tors suggest an interaction between small effective population size (and
founder events) for parasites in the context of patterns of local geographic
isolation. The patchy and unpredictable distributions for some anoplo-
cephalines on fine spatial scales may increase the potential for extinction
events over evolutionary time; for example, there are no species of Micro-
cephaloides known across the expanse of Siberia from the Ural Mountains
to the Russian Far East (V. Haukisalmi, Personal Communication). In
contrast, species of Arostrilepis generally are regionally widespread (with
some exceptions) and homogenous in distribution with often large num-
bers of worms within hosts and many infected individuals and species of
arvicolines at local scales. For Arostrilepis, this pattern would suggest sub-
stantially larger effective populations that would be less strongly influ-
enced by fine scale isolation and partitioning of habitats (Hoberg et  al.,
2003). Although Arostrilepis is regionally abundant, species have yet to be
discovered in the Fennoscandian sector of the western Palaearctic.
Considering heligmosome nematodes, the genus Heligmosomoides is
primarily associated with the arvicolines (also occurring in Muridae, Sciu-
ridae and other Cricetidae) and includes about 36 species, of which 14 or
15 occur in the Nearctic; a single species, H. hudsoni is Holarctic in distri-
bution (Durrette-Desset, 1968, 1971; Rausch and Rausch, 1973; Asakawa,
Northern Host–Parasite Assemblages     47

1988). Origin and diversification of this fauna is related to independent

events of biotic expansion from the Palaearctic since the early Pleistocene
and a history of cospeciation with voles and lemmings (Durette-Desset,
1968; Durette-Desset et  al., 1972; Asakawa, 1988). Distributions of spe-
cies among other cricetids are attributed to a history of independent host
switches and diversification, primarily in the Nearctic (Durette-Desset
and Kinsella, 2007).
Aside from the heligmosome nematodes among arvicolines (e.g.
Durette-Desset et  al., 1972; Ryzhikov et  al., 1979), cestodes are the only
apparently high diversity groups of metazoan parasites occurring at high
latitudes. Haukisalmi et  al. (2006) summarised the structure of the arvi-
coline cestode fauna in Beringia and recognised four primary sources or
distributions for species of Paranoplocephala: (1) Holarctic species, (2) wide-
spread Nearctic species, (3) east Beringian endemics and (4) a single species
with a Palaearctic western Beringian distribution. Among the estimated 35
species of Paranoplocephala, the eastern Beringian fauna (13 species) was an
admixture of Nearctic and Holarctic species. A greater number of endemics
occur in the western Eurasian fauna, which appears to parallel diversity
observed for tapeworms in Leporidae, although these latter assemblages
are older than those in arvicolines (Wickström et al., 2005; Haukisalmi et al.,
2006). These distributions are also similar to host and geographic associa-
tions demonstrated for the heligmosomes and suggest the generality of
the drivers and biogeographic relationships linked to arvicolines. There is
evidence of cospeciation (often associated with colonisation as a precur-
sor) for species in Lemmus, Dicrostonyx, Microtus and Myodes ­(Wickström
et al., 2003; Haukisalmi et al., 2006). Additionally, colonisation of emergent
arvicoline lineages appears as a primary mode of diversification among
species of Anoplocephaloides (Haukisalmi et al., 2009).
Patterns evident among either anoplocephalids or hymenolepidids
indicate (1) multiple historical events of intercontinental geographic
expansion spread over extended time frames spanning the late Pliocene
and Pleistocene, (2) episodic expansion and contraction of ranges during
glacial and stadial cycles and (3) recurrent fragmentation of host–parasite
assemblages where small effective population size for isolated parasite
populations would constitute drivers for divergence and allopatric specia-
tion (Haukisalmi and Henttonen, 2001; Haukisalmi et al., 2001; Wickström
et al., 2001, 2003; Haukisalmi et al., 2006, 2009). Associations reflect some
instances of cospeciation, although host colonisation and subsequent par-
asite speciation may have occurred as a consequence of isolation of sym-
patric host populations in refugial zones of varying extent and duration.
The temporal faunal mosaic with overlapping elements established across
Beringia over extended time frames indicates the potential for complex
assemblages of hosts and parasites developed through zones of primary
and secondary contact (Hoberg and Brooks, 2008, 2010).
48     Eric P. Hoberg et al.

1.4.4. Faunas associated with Artiodactyla

• The parasite groups: Nematoda – Strongylida, Trichostrongylina
(Molineoidea – Nematodirinae; Trichostrongyloidea – Ostertagiinae);
Metastrongylina (Dictyocaulidae, Protostrongylidae); Spirurida
(Filarioidea). Taxonomy is consistent with Durette-Desset et al. (1994),
Anderson (2001) and Chilton et al. (2006) (Table 1.7).
• The host groups: Artiodactyla – Cervidae (Capreolinae – Alces, Odocoi-
leus, Rangifer; Cervinae – Cervus); Bovidae (Antilopinae – Saiga; Bovi-
nae – Bison; Caprinae – Oreamnos, Ovibos, Ovis). Taxonomy consistent
with Wilson and Reeder (2005) and Hernández Fernández and Vrba
Although characterised by relatively low diversity, some pecoran rumi-
nants (for example, caribou and reindeer) and their parasites are promi-
nent members of high-latitude communities across the circumpolar region
(e.g. Halvorsen, 1986; Hoberg et al., 1995, 1999; Halvorsen and Bye, 1999;
Irvine et al., 2000; Hoberg et al., 2001; Hoberg, 2005a; Kutz et al., 2012).
Diversification among the ruminants has been strongly influenced by epi-
sodes of climatological variation and habitat perturbation extending from
the Oligocene to middle Pliocene (Hernández Fernández and Vrba, 2005).
Distributions for those species now occurring at high latitudes were deter-
mined predominantly during the Pliocene and Pleistocene coincidental
with cycles of glaciation and a series of independent expansion events
from Eurasia into North America during the Miocene, Pliocene and Pleis-
tocene (e.g. Guthrie, 1968a; Guthrie and Matthews, 1971; Kurtén and
Anderson, 1980; Guthrie, 1982; Webb, 2000). Patterns of geographic colo-
nisation for ungulate assemblages indicate differential and independent
events during successive glacial stages in the Pleistocene and account for
most extant diversity (excluding Antilocapridae and Camelidae) (Hernán-
dez Fernández and Vrba, 2005). Members of Cervidae and Caprinae are
dominant in the North American fauna.
Across northern habitats of the Nearctic and Palaearctic in the late Ter-
tiary and Pleistocene, a widely distributed assemblage of ungulates was
characterised by greater diversity and more extensive sympatry relative
to faunas in the Holocene (Guthrie, 1982; Vereschagin and Baryshnikov,
1982; Guthrie, 1984, 2006). At maximum levels of diversity near the ter-
mination of the Pleistocene, this assemblage included bovids (Bison spp.,
Bos, Saiga, species of Ovis and Ovibos), cervids (Cervus, Rangifer and Alces),
antilocaprids and camelids (Kurtén, 1968; Kurtén and Anderson, 1980).
More extensive sympatry and higher diversity in a regime of environ-
mental perturbation are consistent with drivers for host colonisation by
parasites (e.g. Hoberg and Brooks, 2008; Hoberg, 2010). In contrast, near
the termination of the ultimate glacial cycle, habitat disruption resulted in
range restriction, limited sympatry and extinction (Guthrie, 1984).
Northern Host–Parasite Assemblages     49

TABLE 1.7  Species diversity and biogeography for exemplar helminth parasites among
ungulates in the Arctic and Subarctic, exploring assemblages influenced by episodic
climate change and geographic expansion in the Pliocene and Quaternary. Species
richness is reflected for global diversity, distributions across the Holarctic and those
that are endemic to either the Nearctic or the Palaearctic

Parasite taxon Host association Distribution Species diversitya Processesb

Marshallagia Bovidae/­ Holarctic (12+G/1H/1N/10P) GE, HC, R
spp. Cervidae
Orloffia spp. Bovidae/­ Holarctic (3+G/0H/1N/2P) GE
Ostertagia Bovidae/­ Holarctic (12+G/1H/1N/10P) GE
spp. Cervidae
Teladorsagia Bovidae/­ Holarctic (3+G/1H/0N/2P) GE, R
spp. Cervidae
Trichostron- Bovidae/ Holarctic (30+G/0H/7N/23P) GE, HC
gylus spp.c Cervidae
Nematodirus Bovidae/­ Holarctic (50+G/7H/7N/26P) GE, HC
spp. Cervidae
Nematodirella Bovidae/­ Holarctic (6G/3H/1N/2P) GE, HC
spp. Cervidae
Dictyocaulus Bovidae/­ Holarctic (7G/1H/0N/6P) GE
Protostrongy- Caprinae Holarctic (23G/0H/3N/20P) GE
lus spp.
Parela- Cervidae Nearctic (3G/0H/3N/0P) GE, HC, R
phostrongy- ­(Caprinae) (2 eastern Beringia)
lus spp.
Varestrongy- Cervidae Holarctic (9G/0H/2N/7P) GE, HC
lus spp. ­(Caprinae)
Onchocerca Cervidae Holarctic (17+G/0H/1N/16P) GE
Rumenfilaria Cervidae Holarctic (1H) GE
Setaria spp. Bovidae, Holarctic (47+G/0H/3N/44P) GE, HC
a  Species diversity relative to regions: G = global, H = Holarctic, N = Nearctic, P = Palaearctic.
b  Processes include geographic expansion = GE; host colonisation = HC; refugial effects = R.
c  Nearctic Trichostrongylus are primarily in rodent or leporid definitive hosts.

d  Filarioid diversity also includes species distributed outside of the Palaearctic region in the Old World.
50     Eric P. Hoberg et al.

In the Nearctic, the earliest cervids are recognised in the fossil record
about 5Ma (Webb, 2000) although divergence and diversification among
Cervinae and Capreolinae had ensued in the early Miocene near 23Ma
(Hernández Fernández and Vrba, 2005). Early diversification within
Odocoileini and Rangiferini also may have occurred in the Palaearctic.
Odocoileini, Rangiferini, Cervini and Alceini have had independent tra-
jectories in North America, representing successive waves of expansion
and establishment (Webb, 2000).
Reindeer (Eurasia) and caribou (North America) are the most promi-
nent of the high-latitude cervids. Rangifer represents a Beringian endemic
over the past 2 Myr that initially diversified in this region with second-
ary isolation north and south of the continental glaciers in the Nearc-
tic (Guthrie and Matthews, 1971; Flagstad and Røed, 2003; Cronin et al.,
2005; McDevitt, et  al., 2009). During the late Pleistocene, a continuous
population occurred across Beringia and Eurasia. Additionally, one
or more discrete refugial populations existed south of the Laurentide
in North America. Isolation resulted in barren-ground ecotypes in the
north and woodland forms in the south with secondary contact occur-
ring along ecotones through expansion in postglacial time (Flagstad and
Røed, 2003). During the Wisconsinan, southern caribou populations were
in sympatry with Odocoileus and other ruminants. Notably, reindeer and
caribou are highly vagile, migratory and have the capacity to disperse
over large distances. In contrast, moose (or elk, Alces) was widespread
in northern Eurasia from the middle to late Pleistocene (Kurtén, 1968;
Kurtén and Anderson, 1980) but arrived in the Nearctic only about 15Ka
and did not attain a broad range in North America until the Holocene
(Guthrie, 1968a; Kurtén and Anderson, 1980; Hundertmark et al., 2002;
Lister, 2004). Historically, moose occurred at low densities and were the
least common ungulate within the Pleistocene assemblage of Beringia
(Guthrie, 1968a).
Diversification within Caprinae (containing Caprini and Rupicaprini)
extends to 14Ma in Eurasia (Hernández Fernández and Vrba, 2005). Cap-
rini (Ovis spp.) and Rupicaprini (Oreamnos) are not known in the Nearc-
tic until Nebraskan to Kansan time about 600–300Ka. Pachycerine sheep
initially became established in North America at this time, followed by
expansion to the south tracking deglaciation during the Yarmouth inter-
stadial about 300–200Ka (Kurtén and Anderson, 1980). Ovis nivicola in
Siberia and Ovis canadensis + O. dalli resulted from this sequential history
of expansion and isolation. Populations of bighorn and Dall’s sheep have
not apparently been in contact since the mid-Pleistocene about 250Ka
(Loehr et  al., 2006). Populations of O. canadensis in the southern Rocky
Mountains assumed their current range with northward dispersal into the
western Cordillera starting near 15Ka (Geist, 1985). Dall’s sheep are recog-
nised in Beringia initially in the Sangamon and survived the ultimate
Northern Host–Parasite Assemblages     51

Pleistocene glaciation in this region and in isolated refugial zones situated

between the Laurentide and Cordilleran ice masses in British Columbia
and the Mackenzie Mountains (Worley et al., 2004; Loehr et al., 2006). Con-
tact apparently occurred between populations of O. canadensis and O. dalli
in the British Columbian refugium, although the former did not survive
the terminal Pleistocene in the Subarctic (Loehr et al., 2006). This complex
history has implications for helminth faunas distributed in wild sheep and
mountain goats extending into the Subarctic and Arctic (e.g. Hoberg et al.,
1999; Hoberg, 2005a).
Mountain goats, Oreamnos americanus, have a biogeographic history
that parallels that of Ovis spp. in North America with discrete northern
and southern subspecies and evidence of isolation in a northern refugium
in British Columbia (Harington, 1971; Shafer et al., 2011). In contrast, mus-
koxen, Ovibos and Symbos, expanded into Beringia during Kansan time
(900–700Ka) and occurred in periglacial habitats south of the Laurentide
and in Beringia during the penultimate glacial stages; Ovibos moschatus
survived the Pleistocene across the Holarctic, but in the Holocene became
extinct in the Palaearctic, and were widely extirpated in Alaska and Can-
ada during the nineteenth century. Muskoxen expanded from the central
Canadian Arctic into Greenland only in the mid Holocene about 4.5Ka
(contrasting with caribou that were present during the last interglacial
stage) (Campos et  al., 2010). Other bovids that were transiently present
in northern latitudes of the Pleistocene included Saiga tatarica and species
of Bison and Bos, the sole representatives, respectively, of the Antilopinae
and Bovinae (Kurtén and Anderson, 1980; Harington, 1990; Harington
and Cinq-Mars, 1995).
The northern nematode fauna in ungulates has its origins in Eurasia.
Greatest diversity of nematode groups in central Eurasia indicates early
radiations, already associated with development of distinct faunas includ-
ing representatives of Strongylina (Strongyloidea), Trichostrongylina
(Nematodirinae – Nematodirus and Nematodirella, Ostertagiinae – Marshallagia,
Teladorsagia, Ostertagia, Orloffia) and Metastrongylina (Dictyocaulidae –
Dictyocaulus; Protostrongylidae – Protostrongylus, Umingmakstrongy-
lus, Varestrongylus and Parelaphostrongylus) (Boev, 1975; Hoberg, 2005a).
Expansion into the Nearctic occurred as a series of independent events at
intercontinental scales with distributions secondarily influenced by epi-
sodes of intracontinental isolation in the late Tertiary and Pleistocene. In
this regard, Beringia and associated refugial systems appear as the centre
of evolution for an Arctic-adapted nematode fauna in ungulates with spe-
cific tolerances for transmission in extreme environments characterised by
seasonally low temperatures and varying degrees of desiccation. The late
geographic colonisation of the Nearctic in evolutionary time, however,
is consistent with the relatively limited number of genera and species of
nematodes represented among ruminants at high latitudes of this region
52     Eric P. Hoberg et al.

(e.g. Hoberg, 2005a). Further, groups such as the Haemonchinae, Coo-

perinae and Trichostrongylinae are either absent or poorly represented
in the endemic Nearctic fauna, apparently reflecting the cold insular and
xeric habitats and sharply defined seasons that constituted a filter on dis-
tribution (e.g. Hoberg et  al., 2004; Hoberg, 2005a; Hoberg et  al., 2008a).
For example, Ashworthius, Mazamstrongylus, Orloffia and Trichostrongylus
have Holarctic distributions but are confined to temperate latitudes, with
reduced diversity in the Nearctic, and are not represented in the high-
latitude fauna (Hoberg, 1996; Hoberg et al., 2001, 2002a).
Initial radiation of Nematodirinae, including Nematodirus, occurred in
Eurasian Caprinae during the middle to late Miocene, with subsequent
colonisation of cervids consistent with the high diversity for this genus in
the Palaearctic (Hoberg, 1997b, 2005a). Other than those species that have
been translocated with domestic ruminants, there are few that occupy
Holarctic ranges (Hoberg et  al., 2008b). Distinct assemblages of species
occur in Cervidae and Caprinae, indicative of discrete events for geo-
graphic colonisation (Hoberg, 2005a). In parallel, species of Nematodirella
were influenced by multiple dispersal events across Beringia with Cervi-
dae and Bovidae (Lichtenfels and Pilitt, 1983; Hoberg, 2005a).
Metastrongyline nematodes were also influenced by independent
expansion from Eurasia and isolation in North America among both Cap-
rinae and Cervidae (Carreno and Lankester, 1994; Hoberg et al., 1995; Car-
reno and Hoberg, 1999). Low species diversity characterises these groups.
For example, a single species of Dictyocaulus (D. eckerti) appears to be
distributed at high latitudes in caribou/reindeer and muskoxen (Divina
et al., 2002; Höglund et al., 2003). This association initially suggests arrival
in North America linked to such late colonisers as moose near the termi-
nation of the Pleistocene. A consistent 4% divergence in the internal tran-
scribed spacer region 2 (ITS-2) of ribosomal DNA for specimens attributed
to D. eckerti in the Nearctic and Palaearctic, however, suggests a longer
period of isolation (E. Hoberg and A. Abrams, unpublished data).
Among other metastrongylines, the protostrongylid lungworms
are represented by three genera, Protostrongylus (among wild sheep),
Umingmakstrongylus (in muskoxen) and Varestrongylus (in caribou,
moose and muskoxen). Diversity for the lungworms, particularly spe-
cies of Protostrongylus, is greatest among Eurasian Caprinae, reflect-
ing the centres for origin and radiation of these parasites (Boev, 1975;
Carreno and Hoberg, 1999). Distribution of genera and species in the
Nearctic all reflect a complex history of geographic and host colonisa-
tion extending from the Pleistocene to recent events reflecting ongoing
ecological shifts at high latitudes (Hoberg et al., 2002b, Hoberg, 2005a;
Jenkins, 2005; Kutz et al., 2007). Species of Protostrongylus in wild sheep
are components of a broader Holarctic–Eurasian assemblage, and
distributions in North America may reflect expansion with ancestral
Northern Host–Parasite Assemblages     53

species of Ovis (Jenkins, 2005). Unlike Parelaphostrongylus or Varestrongylus

where gene flow for parasites may be mediated by several host species,
lungworms such as P. stilesi circulate almost solely within Ovis, and at
lower latitudes in Ovis and Oreamnos. The limited vagility and isola-
tion demonstrated for populations of O. dalli would be predicted to
drive considerable structure in parasites isolated both within mountain
systems and on high-altitude sky islands. For example, partitioning of
local parasite populations would be predicted by distance across the
Brooks Range, Alaska Range (from the Chugach to near the Lake Clark
region), isolated mountain blocks in the Alaskan interior (Yukon Char-
ley and White Mountains) and across the Richardson Mountains and
Mackenzie Mountains of Canada (e.g. Loehr et  al., 2006: E.P. Hoberg
and K. Beckmen, unpublished data). Additionally, contemporary range
expansion and host switching for P. stilesi was documented in a zone
of contact for Dall’s sheep and muskoxen in Alaska and the potential
for reciprocal exchange of parasites between subspecies of Ovibos at the
Mackenzie River ecotone has been predicted (Hoberg et al., 2002a; Kutz
et al., 2004).
Considering other lungworms, Umingmakstrongylus has been regarded
as a relictual genus now endemic to the Central Arctic of Canada where it
appears as a host-specific parasite in muskoxen (Kutz et al., 2001a). Although
currently geographically limited, U. pallikuukensis may have had a more
extensive geographic distribution prior to extinction and extirpation of mus-
koxen populations in both Eurasia and North America (Hoberg et al., 1995;
Campos et al., 2010). In contrast, a single species attributable to Varestrongylus
appears to be widespread at high latitudes from Alaska to Labrador (Kutz
et al., 2007). A primary host association with cervids (caribou) and second-
ary host switching to muskoxen in zones of recent contact has been postu-
lated for this undescribed species. Similar to other protostrongylids, species
of Varestrongylus are prominent parasites of Eurasian ungulates (Boev, 1975).
Protostrongylid muscleworms include the elaphostrongylines and
genera restricted to either the Palaearctic (Elaphostrongylus; except for
E. rangiferi introduced to Newfoundland) or the Nearctic (Parelaphostrongylus)
(Lankester, 2001). The subfamily radiated principally with cervid hosts,
underwent expansion into the Nearctic with Odocoileini and subsequently
diversified among species of Odocoileus south of the Laurentide ice (Platt,
1984; Carreno and Lankester, 1994). At high latitudes of the Nearctic, two
species, Parelaphostrongylus andersoni (in caribou) and P. odocoilei (in wild
sheep, mountain goats and woodland caribou) are currently known. Evi-
dence for south to north expansion tracking continental deglaciation either
in the post-Pleistocene or in an earlier interglacial is seen in the distribu-
tions of Parelaphostrongylus odocoilei in Dall’s sheep, mountain goats and
woodland caribou (Kutz et al., 2001b; Jenkins et al., 2005) and P. andersoni,
which is widely distributed among subspecies and herds of Rangifer
54     Eric P. Hoberg et al.

tarandus (Lankester, 2001; Asmundsson et al., 2008). Both species are pri-
mary parasites among species of Odocoileus at temperate latitudes but
through northward geographic expansion and host switching now have
considerably more extensive ranges in North America extending into the
Subarctic and Arctic. The distribution of P. odocoilei excludes the Brooks
Range of Alaska and the Richardson Mountains of the Yukon and North-
west Territories suggesting relatively recent expansion and host switching
from mule deer or black-tailed deer in zones of contact following degla-
ciation of the Cordillera. Alternatively, data from phylogeographic studies
using mitochondrial cytochrome oxidase I (COI) may indicate two centres
of diversity, with (1) a southern population primarily in O. hemionus and
(2) a northern population coinciding in part with the former Mackenzie
refugium that was intermittently present on the northern margin of the
Cordillera during the last glacial maximum (I. Asmundsson, E. Hoberg,
A. Abrams and E. Jenkins, unpublished data) (Worley et  al., 2004; Loehr
et al., 2006; Shafer et al., 2010). Such a partition in COI would be consistent
with a pattern of earlier isolation in contrast to expansion and host coloni-
sation from deer during the Holocene. Complex patterns of biogeography
may relate to development of independent contact zones for hosts both in
the unglaciated coastal zone extending on the western margin of the Cordil-
lera and in continental refugial zones between the Cordillera and Lauren-
tide (e.g. Shafer et al., 2010). Philopatric behaviour of thinhorn sheep and
limited postglacial expansion from refugia may further explain the absence
of parasites at higher latitudes.
In contrast to P. odocoilei, populations of P. andersoni appear to be
poorly differentiated, and there is no strong genetic signal demonstrat-
ing isolation north and south of the continental glaciation (E. Hoberg
and I. Asmundsson, unpublished data). A postulated host switch from
white-tailed deer to caribou in a southern refugium during the ultimate
glaciation, subsequent postglacial expansion and a shift from woodland
to barren-ground caribou in the Holocene is consistent with this distribu-
tion. Additionally, expansion during the Holocene explains the apparent
absence of these parasites in once continuous populations of barren-
ground caribou and reindeer, which extended from Beringia into Eurasia
during the late Pleistocene.
Refugial effects are evident in the distributions of both gastrointestinal
and pulmonary parasites in ungulates. Complexes of putative cryptic spe-
cies such as those apparent in Teladorsagia and possibly other Ostertagiinae
including Marshallagia spp. among free-ranging Caprinae are consistent
with a history of range fragmentation and recurrent isolation for hosts and
host species across the late Pleistocene (Hoberg et al., 1999; Hoberg et al.,
in press-b). Thus, T. boreoarcticus in muskoxen represents a member of a
complex that may include additional species in Ovis dalli, O. canadensis
and Oreamnos americana. The distribution for a recently recognised species
of Marshallagia in mountain goats (see Lichtenfels and Pilitt, 1989) appears
Northern Host–Parasite Assemblages     55

to be consistent with a history of refugial isolation and contact with

wild sheep in the late Pleistocene (Hoberg et al., in press-b; Shafer et al.,
2010, 2011).
In contrast, Ostertagia gruehneri is not predicted to demonstrate a signal
for refugial isolation in reindeer and caribou. This ostertagiine is one of
few Holarctic species and may not be strongly differentiated at the popu-
lation level in the Palaearctic and Nearctic in parallel to phylogeography
for its primary Rangifer hosts. Further, extensive mixing of barren-ground
and woodland caribou populations following deglaciation would also
suggest associated patterns of gene flow for parasites. It is not known,
however, whether populations of this ostertagiine are partitioned with
respect to identified herds or ecotypes of caribou in the Nearctic. These
hypotheses remain to be examined based on phylogeographic compari-
sons of parasite populations.
Data for the distribution of filarioid nematodes including species of
Rumenfilaria, Setaria and Onchocerca at high latitudes are patchy and incom-
plete. These vector-borne nematodes appear most often in association with
cervids including caribou and moose in North America (Dieterich and
Luick, 1971). Diversity in these genera across the high latitudes is poorly
understood and it is not clear if single species are widespread in the Hol-
arctic (e.g. Becklund and Walker, 1969; Nikander et al., 2006); for example,
the conspecificity of Setaria tundra in the Palaearctic and S. yehi in the Nearc-
tic, which circulate primarily in cervids, remains unresolved. Further, pub-
lished records of Rumenfilaria in North America are limited to the original
description, although these nematodes are likely to have a broad distribu-
tion coincidental with moose definitive hosts (Lankester and Snider, 1982).
Confounding challenges to understanding historical associations and
the development of faunal structure emerge from cryptic species and
hidden diversity. The latter is an issue of incomplete or insufficient sam-
pling of the northern ungulate fauna (Kutz et al., 2012). It is demonstrated
by the discovery of one new genus and two species of protostrongylids
(Hoberg, et  al., 1995; Kutz et  al., 2007), and two species of ostertagiines
(Hoberg et  al., 1999; Hoberg et  al., in press-b). Further, considerably
broader geographic distributions discovered for such protostrongylids as
P. odocoilei in Dall’s sheep and woodland caribou demonstrate the need
for extensive survey and inventory (Kutz et al., 2001b; Hoberg et al., 2003;
Jenkins et al., 2005; Hoberg et al., 2008a). Hidden diversity in conjunction
with assemblages of cryptic species (Pérez-Ponce de León and Nadler,
2010), as revealed among the ostertagiine nematodes, serve to confuse
explanations about the origins and distributions of parasite diversity
in space and time (e.g. Hoberg et al., 1999, 2001). As shown in northern
systems, the effects of refugia and peripheral isolation of host and para-
site populations may be especially pervasive and definition of these pro-
cesses will remain elusive in the absence of fine scale phylogeographic
approaches (e.g. Waltari et al., 2007b; Shafer et al., 2010).
56     Eric P. Hoberg et al.

Translocations of reindeer and muskoxen over the past century may

also have an influence on species diversity and population structure for
nematode faunas in ungulates (MacDonald and Cook, 2009; Rausch and
Baldwin, 2002). These may have resulted in introductions for parasites of
muskoxen or reindeer into high-latitude systems in Alaska and Canada
from various sources in eastern Eurasia, Fennoscandia and Greenland with
the development of mosaic faunas at some localities during the past 100
years (Hoberg et al., 1999; Hoberg, 2010; Kutz et al., 2012). Consequently,
there is a need for population-level assessment of all constituents of this
diverse parasite fauna. For example, preliminary data for Teladorsagia nem-
atodes in an introduced population of muskoxen near Aklavik, Northwest
Territories, Canada, revealed a low level of divergence in the ITS-2 region
of ribosomal DNA relative to those parasites in an historically endemic and
isolated host population (E. Hoberg, K. Galbreath and S. Kutz, unpublished
data). The basis for this genetic variation remains unknown, however, and
sampling has been insufficient to completely explore these relationships.
As historical analogues for understanding environmental change,
certain nematodes among ungulates have already been demonstrated as
robust indicators of the role of climatological processes as determinants
of distribution (e.g. Kutz et  al., 2005; Jenkins et  al., 2006; Hoberg et  al.,
2008b). Distributions of protostrongylids appear strongly tied to ambi-
ent temperature and controls on development for larval stages as dem-
onstrated for Umingmakstrongylus and some species of Parelaphostrongylus
and Protostrongylus. Responses associated with thresholds for develop-
ment, temperature tolerances and resilience are critical limiting factors
for distribution and persistence, both historically and in ecological time
(e.g. Hoberg, 2005a). Understanding these physical controls on distribu-
tion provides insights about faunal structure through the Pleistocene and
a baseline for predicting the outcomes of ecological perturbation in the
current regime of climate warming. The latter has been shown associated
with tipping points in development and changes in transmission dynam-
ics for U. pallikkuukensis among muskoxen in the Central Canadian Arc-
tic and may be a driver for ongoing range expansion for parasites in the
region (Kutz et al., 2005; Hoberg et al., 2008b; Kutz et al., 2012).

1.4.5. Human interfaces and occupation of the North

Palaeolithic hunter-gatherers were present near the Arctic Circle in Sibe-
ria by about 40Ka and subsequent human expansion into high latitudes
of western Beringia during the late Pleistocene about 32Ka was the pre-
cursor for occupation of the Western Hemisphere following the peak of
the last glacial maximum (18–22Ka) (Hoffecker et al., 1993; Dixon, 2001;
Goebel et al., 2008; O’Rourke and Raff, 2010). Multiple expansion events
following different pathways may have led to (1) occupation of the Pacific
Northern Host–Parasite Assemblages     57

coastal zone near 14–13.5Ka, (2) dispersal across near coastal zones of the
low Arctic to eastern North America by 14Ka, (3) colonisation of interior
North America via the deglaciated ice-free corridor after 11Ka and (4) col-
onisation of the Aleutian archipelago after 7–8Ka (Dixon, 2001; O’Rourke
and Raff, 2010; Balter, 2012). Although people had been distributed across
high-latitude environments of the Old World, occupation of Beringia,
secondary colonisation of North America and most recently Greenland
occurred sequentially and over an extended time frame from 15 to 4.5Ka
(Dixon, 2001; Goebel et al., 2008).
Pathways for human migration appear initially to be linked to the Ber-
ing Land Bridge. A marine route would provide access to uninterrupted
intertidal zones connecting Eurasia and North America that may have
also included coastal refugial habitats of southeastern Alaska where inver-
tebrates, fishes and marine mammals and birds represent potential prey
(Heaton et al., 1996; Dixon, 2001). In contrast, a terrestrial route would have
facilitated access to assemblages of large mammals, migratory waterfowl
and anadromous fishes as potential prey (Yesner, 2001; Guthrie, 2006). Ter-
restrial- versus marine-oriented migration routes, and later regions occu-
pied by indigenous populations, would influence sources and availability
of potential food, prevailing foraging industries and relative exposure to
different parasite groups (Rausch, 1974).
Arrival of people at high latitudes of the Nearctic about 15Ka altered
the interface for parasites, pathogens and disease in humans, associated
commensals such as dogs and potentially some assemblages of free-
ranging mammals (Rausch, 1972). People influenced parasite diversity
through (1) introduction or facilitation of new geographic distributions
for specific human pathogens (e.g. Enterobius vermicularis and D. latum);
(2) occupation of new ecological settings resulting in exposure to zoonotic
infection from novel assemblages of vertebrate and invertebrate hosts and
parasites, facilitated by local subsistence food chains, water contamina-
tion or proximity, and (3) direct and indirect effects on ecosystem structure
that determined the continuity and persistence of particular assemblages
of hosts and parasites.
Immigrants to North America in the late Pleistocene and early Holo-
cene would have had a long historical association with parasites acquired
through local foraging and the dynamics of food chains (Babbot et  al.,
1961; Cameron and Choquette, 1963; Rausch, 1974; Bouchet et al., 1999).
Marine foraging industries would lead to exposures for tapeworms such as
Diphyllobothrium and Diplogonoporus (from marine fishes), intertidal dige-
neans including Cryptocotyle, Stictodora (and other heterophyids), Micro-
phallus and Maritrema (intertidal demersal fishes and mollusks), anisakine
nematodes including Anisakis, Pseudoterranova and Contracaecum (from
pelagic marine fishes and anadromous fishes), the muscle dwelling Trichi-
nella (from polar bears, walrus and beluga) and possibly acanthocephalans
58     Eric P. Hoberg et al.

in the genera Corynosoma and Bolobosoma (marine fishes). Aquatic food

resources, and specifically both freshwater and anadromous fishes, are
a source for Diphyllobothrium, Schistocephalus, Nanophyetus and Metorchis.
Terrestrial food sources would be associated with infections from Trichi-
nella (brown bears and black bears) and the apicomplexan Toxoplasma gon-
dii (ungulates, carnivores). These latter parasites are often associated with
marine or terrestrial apex predators exploited in subsistence food chains
(e.g. Jensen et al. 2010).
Local contamination of village sites, specifically by working, or sledge
dogs has represented a substantial source for infections by tapeworms and
nematodes (Rausch, 1974; Rausch and Fay, 2011). For example, zoonotic
infections attributable to E. multilocularis and E. granulosus were facilitated
by significant fecal contamination in permanent villages that were increas-
ingly occupied (in Alaska) after the late1800s. The latter parasite also has
had a strong association with either ungulate hunters or reindeer herd-
ers across the north, in situations characterised by uncontrolled access by
dogs to carcasses of cervid intermediate hosts in conjunction with poor
sanitation (Rausch, 1967). In contrast, the transmission of E. multilocularis
in rodent–canid assemblages was enhanced by synanthropic cycles (dogs
and commensal voles) and development of hyperendemic foci for human
infection in permanent village sites (Rausch and Fay, 2002). Circulation of
these taeniids increasingly contrasted with the historical situation where
people encroached but did not substantially disrupt the structure of natu-
rally occurring host–parasite assemblages (Rausch, 1972). Further, histori-
cal levels of infection pressure for E. multilocularis (and E. granulosus) in
people may have been reduced by a typically nomadic life style where
excessive fecal contamination by dogs in food or water resources would
have been minimised (Rausch, 1951, 1972, 1974).
Infections by the ascaridoid, Toxascaris leonina, are also maintained
in the same synanthropic foci as those of E. multilocularis where levels
of infection among dogs and voles (and contamination) in village sites
may exceed that observed under natural conditions in wild canids (Salb
et al., 2008; Rausch and Fay, 2011). Toxascaris leonina is a prevalent para-
site in either foxes or dogs at high latitudes and may circulate through
arvicoline rodents as intermediate/paratenic hosts. Infections by larval
T. leonina are considered to be the source of eosinophilia observed in people
on St Lawrence Island, Alaska, and perhaps other areas of the north. The
advent of motorised transportation replacing sledge dogs in the 1960s
and 1970s has led to a reduced potential for human infection by both
Echinococcus and Toxascaris in northern villages (Rausch and Fay, 2011).
Considering helminth zoonoses in general, humans have been primar-
ily dead-end or terminal hosts for parasites circulating in free-ranging
or commensal mammals and other vertebrates. In this sense, humans
only rarely contributed directly to local or regional maintenance of these
Northern Host–Parasite Assemblages     59

parasites, where infections were a consequence of passive behaviour linked

to foraging, food habits or exposure by contact or contamination in the
absence of sanitation (Cameron and Choquette, 1963; Jenkins et al., 2011).
An exception may be D. latum that appears to be dependant on humans for
perpetuation of transmission in Alaska (Rausch and Hilliard, 1970).
Species of Diphyllbothrium circulate in strictly aquatic (piscivorous birds
or mammals as definitive hosts), marine (pinnipeds, cetaceans and fishes)
or aquatic/marine cycles (Rausch et al., 2010). In the north, human infec-
tions by particular species are linked to these pathways (Rausch and Hill-
iard, 1970). The earliest documented association with people is from Peru
about 4.5Ka, representing infection by species circulating in pinnipeds.
These cycles are likely the sources of infection of early immigrants into
North America during the Quaternary (Bouchet et al., 1999). This contrasts
with humans as primary hosts such as that implied for D. latum in con-
temporary Alaska (Rausch et al., 1967). Did D. latum expand across Berin-
gia with early human inhabitants of high latitudes or did it arrive later to
become established in focal localities associated with European exploration
and settlement, particularly Russian expansion in the 1700s (Rausch, 1974)?
Transmission pathways represent continuous associations for humans
and pathogens that have extended since initial occupation through the
Holocene to the present (Rausch, 1974). Infection routes for human-associ-
ated pathogens, which characterised the last 10,000 years, have been rapidly
modified over the past century. Among the estimated 4 million residents
of the circumpolar north, indigenous peoples now represent only about
10% of the total population at high latitudes, signifying a demographic
shift to relative dominance by those arriving from the outside (Anisimov
et al., 2007). Shifts from nomadic to sedentary life styles may have initially
increased infection pressure for some synanthropic assemblages of para-
sites (Rausch, 1951, 1972, 1974). Alteration in diets away from subsistence
resources and traditional foods has also reduced levels of infection in
some situations but concurrently has raised new challenges and problems
for health of native peoples. Food security and availability may be increas-
ingly challenged by new patterns of infection and abundance for parasites
and diseases in traditional food animals including muskoxen and caribou
(Hoberg et  al., 2008b; Kutz et  al., 2009b). Changing demographics have
substantially altered historical linkages for transmission and patterns of
infection pressure for parasites and pathogens at the animal–human inter-
face. Ironically, some infections of Diphyllobothrium now reported in west-
ern Europe are attributed to the importation of salmon from other regions
of the world (Scholz et al., 2009).
As people became mediators of ecosystem structure through local and
regional hunting and fishing practices, there would have been an emerg-
ing influence on species diversity, abundance, distribution and continu-
ity of parasite assemblages, not simply zoonoses. For example, parasite
60     Eric P. Hoberg et al.

faunal diversity would have been directly influenced by late and post-
Pleistocene megafaunal extinctions, some of which have been attributed
to human hunting or to interactions between anthropogenic causes and
climate change (Barnosky et al., 2004; Guthrie, 2006; Lorenzen et al., 2011;
Waters et  al., 2011). Further, in contemporary time, human-mediated
translocation, introduction and establishment of hosts and parasites over
the past century have altered the distributions for helminths and other
pathogens in some carnivores and ungulates (Hoberg, 2010; Hoberg et al.,
in press-a). The impact of resulting mosaic faunas remains to be identified
(Hoberg et al., 2008a; Hoberg, 2010).



There is a generality for low diversity in terrestrial host–parasite systems at

high latitudes. Although at first these patterns are intuitive, closer inspec-
tion has some interesting implications that are connected to a history of
expansion from Eurasia into North America and further south into the
Neotropical zone. Essentially, there is a longitudinal gradient in diversity,
an historical legacy of recurrent or episodic geographic expansion and col-
onisation, which appears in most complex host–parasite systems. Species
richness within respective helminth groups is greatest in Eurasia, less in
North America and minimal in the Arctic, or alternatively, there is a gra-
dient with a gap at high latitudes (Fig. 1.6). The gap of minimal diversity
represents those taxa that could not successfully colonise high latitudes
or that because of thresholds and tolerances and narrow resilience were
secondarily eliminated through local or regional extinction in regimes of
rapid environmental change (e.g. Barker et al., 2011). The gradient empha-
sises the ancestral centre of origin for the fauna (Eurasia) and the historical
processes that have been at play in determining diversity downstream.
Aside from the longitudinal gradient, there is a secondary latitudinal
gradient with greatest diversity (for the few Holarctic groups) in temper-
ate latitudes in either Eurasia or North America. For example, there are
15 genera of Ostertagiinae circulating in ungulate hosts globally. Of these,
only 3 genera and 3 or 4 species occur in the Subarctic and Arctic, 2 gen-
era are Holarctic but with a gap at high latitudes and 10 are Old World
(Palaearctic and African). Patterns extend to the species level (Table 1.7),
and for Marshallagia, there is 1 Holarctic species across temperate to high
latitudes, 1 North American and 10 Eurasian species (Hoberg et al., in press-
b). In Ostertagia, only O. gruehneri occurs across the Arctic; one species is
endemic to North America, there are no species shared across regions and
the greatest diversity (about 10 species) is observed in Eurasia. Teladorsagia
boreoarcticus is probably Holarctic, and no other species (of which there
are two additional congeners) occur outside of a history of introduction
Northern Host–Parasite Assemblages     61

FIGURE 1.6  Distribution of helminth faunal diversity and gradients in species richness
resulting from episodic expansion and isolation across Eurasia and North America through
the Beringian region. Among most helminth groups, diversity (species richness) is greatest
in Eurasia (++++), minimal at high latitudes (few Holarctic species +/−) and is reduced in
the Nearctic (++). These patterns, or longitudinal/latitudinal gradients, reflect the down-
stream influence of eastward geographic colonisation over time from regions of ancestral
origin (Eurasia) to secondary centres of diversification (North America). Consequently,
expansion and geographic colonisation across Beringia set the stage for later diversifica-
tion within helminth groups in both the Nearctic and the Neotropical regions.

in North America. Among the nematodirines, there are 6 Holarctic species

of Nematodirus at high latitudes, about 7 from the Nearctic and Neotropi-
cal regions and about 40 restricted to the Palaearctic including those that
have been globally disseminated with movement of domestic artiodactyls
(Kulmamatov, 1974; Hoberg, 2005a). Additionally, in the realm of ungulate
62     Eric P. Hoberg et al.

parasites, many simply never colonised North America coincidental with

their hosts, including gastrointestinal parasites such as Haemonchus, Coo-
peria and Spiculopteragia and protostrongylids represented by Cystocaulus,
Muellerius and others. Intercontinental expansion in the middle to late
Pliocene with cervids may be indicated by the occurrence of Mazamstron-
gylus and Ashworthius in Eurasia and the Western Hemisphere (but not in
the Arctic) under the influence of relatively equitable climate factors and
warm conditions at high latitudes (Hoberg et al., 2004; Robinson, 2011). In
contrast, the distributions for Ostertagia, Teladorsagia, Marshallagia and the
nematodirines were not strongly influenced by climate filters related to
cold and xeric environments later in the Pleistocene.
Considering otherwise Holarctic groups, a gradient for downstream
diversity is also represented among parasites in rodents, lagomorphs and
carnivores and serves to highlight the history of episodic expansion link-
ing ancestral centres of diversification in Eurasia with secondary zones in
North America (Tables 1.4–1.6). A reduction in diversity with geographic
colonisation also indicates the predominant eastward direction for expan-
sion during the Pleistocene (Rausch, 1994; Waltari et al., 2007b). Limited
diversity and the historical mechanisms involved emphasise the unique
nature and relative simplicity of northern host–parasite systems. Further,
and secondarily in some systems, a latitudinal gradient has been superim-
posed, which reflects north–south and south–north expansion, isolation
and diversification particularly in North America (Galbreath and Hoberg,
2012). Among pikas, these patterns for recurrent expansion and isola-
tion have resulted in the origins of substantial diversity in most helminth
groups that secondarily emerged following geographic colonisation from
Eurasia; to some degree, a contrast with a general pattern was observed in
other host–parasite assemblages (Table 1.5).
The apparently unique distribution of diversity downstream from
Eurasia and across Beringia was initially recognised in the history of arvi-
coline rodent faunas (Repenning, 2001). A general or replicated pattern for
species richness now seems evident for complex biological systems across
this geographic arena. We introduce the new term – ‘trans-­Beringian
disjunct distribution’ – for biotic assemblages with largely boreal temper-
ate to Subarctic ranges that retain some limited diversity in Beringia or
high latitudes. The most diverse components of these assemblages are
in temperate Eurasia and temperate North America. Such patterns are
best exemplified among helminth groups in ungulates, rodents and lago-
morphs under the influence of (1) rapid expansion tracking suitable habitat
through Beringia during the Pliocene and Pleistocene; (2) exclusion, extir-
pation or local extinction in east and west Beringia during glacial maxima
and (3) limited postglacial expansion returning to Beringian latitudes as a
function of specific tolerances, developmental thresholds and other biotic
(e.g. distribution of potential intermediate hosts) and abiotic parameters.
Northern Host–Parasite Assemblages     63

Thus, there is an apparent interplay between vagility and ­specialisation

and episodic climatological processes as determinants of species ranges in
these assemblages (Dynesius and Jansson, 2000).

1.5.1. General biogeographic patterns

A history of episodic expansion and isolation under variable regimes of
climate defined by glaciations and interglacial stages, with the origin and
dissolution of refugial zones, emerges as a central driver for patterns of
distribution and diversification of the northern fauna (e.g. Dynesius and
Jansson, 2000; Jansson and Dynesius, 2002; Shafer et  al., 2010). Encom-
passed within this rather general framework, specific examples or models
for these and related processes are evident, constituting a pathway for
exploring the relative roles and interactions of different biogeographic
determinants in space and time.
(1) The standard Beringian model: a) Geographic colonisation of eastern
Beringia from Eurasia across the land bridge coincidental with glacial
maxima during the Pleistocene (or prior to the Pliocene–Pleistocene
boundary); b) subsequent interglacial vicariance of Beringian faunas at
Bering Strait and c) interglacial expansion south into North America,
subsequent vicariance north and south of the Laurentide–Cordillera
with post-Pleistocene expansion to varying extent as a function of refu-
gial effects. Interestingly, the strong phylogeographic discontinuity pre-
dicted at Bering Strait appears shifted westward towards the Kolyma
highlands of Chukhotka near the periphery of western Beringia (e.g.
Galbreath and Cook, 2004); this pattern is emerging as a generality for
a number of mammaliam groups and presumably their parasites.
(2) North American regional southern refugia: During the last glacial,
maximum forested refugial zones (eastern and western) have been
inferred south of the Laurentide. Postglacial expansion in the early
Holocene from south to northwest is postulated from eastern refugia
in North America (e.g. Rangifer, Martes americana, Myodes voles, black
bears, tree squirrels, red fox). Distributions are consistent with early
expansion and occupation of North America by a number of discrete
mammalian lineages by the mid-Pleistocene, followed by extirpa-
tion of high-latitude populations in eastern Beringia or the Arctic.
For example, the history of Soboliphyme in martens exemplifies this
complex process for hosts and parasites (Koehler et al., 2009).
(3) Repopulation of eastern Beringia from Eurasia: Extirpation of some
lineages or populations of mammals in eastern Beringia was followed
in a number of cases by expansion secondarily from Eurasian sources
during glacial maxima. This pattern is exemplified by both caribou/
reindeer and red foxes and some arvicoline rodents and their para-
sites. Thus, Eurasian and Beringian populations were continuous and
64     Eric P. Hoberg et al.

contrast with those expanding from the south, tracking deglaciation

in post-Pleistocene environments. This suggests that many taxa and
species or populations of parasites that are considered to be wide-
spread in the Nearctic from temperate to Subarctic and Arctic lati-
tudes may not be closely related, and some will have greater affinities
to faunas now isolated across Bering Strait in eastern Eurasia.
(4) Return to Beringia: Patterns involve expansion into North America by
the mid-Pleistocene or earlier, occupation of temperate latitudes dur-
ing a subsequent interglacial and isolation and extirpation of northern
populations during the next glacial cycle in the absence of expansion
from Eurasia into eastern Beringia. In this model, repopulation of Berin-
gia occurs from southern refugia prior to the Wisconsinan or ultimate
glaciation, with lineage continuity and diversification encompassing
multiple glacial–interglacial cycles. North American pikas and the
diversification of O. princeps and O. collaris and their complex helminth
fauna are consistent with this scenario (Galbreath and Hoberg, 2012);
additionally, shrews of the species complex represented by Sorex cinereus
demonstrate this association (Demboski and Cook, 2003; Hope, 2011).
(5) Pleistocene (Wisconsinan) expansion from Eurasia: These taxa
represent late arrival on the Beringian scene and include moose, the
northern lineage of red fox and some wolves. In these situations, host
taxa are expected to have parasites with greater affinities to Eurasia
than to North America. Postglacial expansion has been variable, with
moose, for example, coming to occupy the entire breadth of North
America in the Holocene.
(6) Western coastal refugial zones: Distinct glacial refugial zones on the
outer coast of British Columbia and Alaska are consistent with iso-
lation and diversification of hosts and parasites in western insular
habitats. Coastal refugial patterns have been demonstrated for bears,
wolves and Pacific martens (Heaton et  al., 1996; Cook et  al., 2006;
Hoberg et al., in press-a).
(7) Macro- and micro-refugial effects: Habitat structuring and partition-
ing during both glacial maxima and under special circumstances for
particular taxa under interglacial regimes serve to influence patterns
of isolation and diversification for complex host–parasite systems.
Most clearly defined for glacial stages, refugial zones may be large
such as that encompassing Beringia or at very small spatial scales such
as those associated with periglacial habitats (Shafer et al., 2010, 2011).
Isolation in interglacial refugial zones at extreme high latitudes often
in archipelagos (responses related to range contraction during warm
periods) followed by population and geographic expansion during
glacial advances represent special cases for Arctic fox and polar bear.
(8) Radiations and bottlenecks: Pliocene/Pleistocene radiations are appar-
ent for a number of host–parasite assemblages, often followed by local or
regional extinction events or bottlenecks of differing scope and intensity
Northern Host–Parasite Assemblages     65

near the Pleistocene/Holocene transition, particularly among carnivores

and ungulates. Radiations appear to have been influenced by vagility,
gene flow and scales of isolation. The distribution of endemic faunas
reflects the interaction of these factors relative to host group: (1) arvi-
coline parasite faunas exhibit endemism at local to regional scales, (2)
lagomorphs at local to regional scales and (3) carnivores and ungulates
at regional to intercontinental scales. These associations reflect scales of
relative vagility and further may indicate the velocity for expansion and
contraction during range shifts (e.g. Sandel et al., 2011; Arenas et al., 2012).
(9) Beringia as a pass-through for neotropical faunas: Beringia was the
gateway for terrestrial expansion from Eurasia into North America, and
for some taxa, geographic colonisation was not limited to the Nearctic. For
example, felids arrived and diversified initially in South America prior
to the emergence of the Panamanian Isthmus near 8Ma, an event that
may also be linked to the early diversification of Trichinella nematodes
(Johnson et al., 2006; Pozio et al., 2009). In contrast, neotropical distribu-
tions for some ungulate parasites, including Nematodirus and Mazamas-
trongylus, were only established following multiple expansion events
across Beringian and into South America with subsequent host switch-
ing (from cervids to camelids) after 3Ma (Hoberg, 2005a). Likewise, the
underrepresentation of endemic Taenia in the Neotropical region relates
to patterns of expansion across Beringia for canids and felids and even-
tual passage into South America in the late Pliocene and Pleistocene
(Webb and Marshall, 1981; Marshall et al., 1982; Rossin et al., 2010).
(10) Dynamic and episodic invasion: It is evident that expansion events
have had considerable complexity in space and time. Considering the
phylogenetic range of these host–parasite assemblages, geographic
colonisation has occurred over varying spatial and temporal scales.
Respective host groups have been influenced by episodic expansion
(contraction) and isolation on different trajectories (e.g. Sandel et al.,
2011; Arenas et al., 2012). Parasite diversity is influenced under sce-
narios for host expansion and establishment (demographic effects for
hosts), recurrent patterns (origin, number and extent of expansions,
synchronic events), propagule size (abundance and intensity of infec-
tions and numbers of infected hosts disseminating parasites, host den-
sity and dispersion) for invading parasites, and life history constraints
(facilitators and buffers) (Hoberg and Brooks, 2008; Hoberg, 2010).
(11) Faunal mosaics for hosts and parasites: Mosaic structure
(addressed in detail below) or faunal admixtures result from recur-
rent or episodic events of expansion and isolation under a dynamic
for taxon pulses (Hoberg and Brooks, 2008, 2010). Most host–
parasite assemblages in the north represent mosaics assembled over
extended time frames since the late Pliocene and through the Quater-
nary and some with anthropogenic influences in the Holocene (e.g.
Hoberg, 2005a, 2010; Hoberg et al., 1999, in press-a).
66     Eric P. Hoberg et al.

1.5.2. Mechanisms of faunal expansion in space and time

The complexity of processes for faunal expansion serves as a determinant
of geographic and temporal continuity for assemblages of parasites across
phylogenetically disparate host groups (Hoberg, 2005a). Mechanisms of
invasion and geographic colonisation leading to establishment of com-
plex faunas are equivalent in evolutionary and ecological time (Hoberg
and Brooks, 2008, 2010; Hoberg, 2010). This point is emphasised by the
observation of gradients in diversity that are apparent downstream from
Eurasian centres of origin for many assemblages.
Gradients result from invasion in evolutionary and ecological time
and may be manifested as both microevolutionary (population genetics
and diversity) and macroevolutionary (higher taxon, generic and species
richness) phenomena (e.g. Avise, 2000; Torchin et al., 2003). Depletion of
genetic diversity moving away from an ancestral centre is a characteristic
signature of geographic colonisation involving populations and species.
Anthropogenic introductions of hosts or host groups in contemporary
time may also be expected to lead to selective loss of diversity for associ-
ated parasite faunas (Torchin et al., 2003). These are generalities across a
continuum for host–parasite assemblages in source (ancestral areas) and
recipient regions under the influence of episodic expansion and invasive
processes (Hoberg and Brooks, 2010). Thus, from a macroevolutionary
perspective, for nearly every helminth group with origins in Eurasia, the
diversity downstream (following eastward expansion across Bering Land
Bridge) is substantially reduced in the Nearctic. Considerable diversity in
Eurasia is followed (temporally and spatially) by often complete absence
at high latitudes but with considerably lower levels of species richness
distributed at boreal/temperate latitudes in North America. Under a
regime of episodic expansion, both environmental filters (resilence and
tolerance) and temporal dimensions (relative timing of expansion) can
be invoked to explain resulting patterns of diversity. There are few Hol-
arctic species but also few endemics in the Nearctic resulting from post-
expansion isolation and diversification for helminths among lagomorphs
(to some degree excluding Ochotona with a relatively deep history in the
Nearctic), rodents, carnivorans and ungulates. These generalities remain
to be explored for the diverse faunas associated with soricomoprhs across
the Holarctic region (e.g. Kinsella and Tkach, 2009; Binkienė et al., 2011).
Diversity and its association with episodic invasion further establish the
importance of the Berinigian model where recurrent climatological and
environmental processes serving as determinants of faunal diversity can
be defined in space and time.
In northern systems, intercontinental and intracontinental expansions
have been associated with permissive environmental regimes, host–parasite
assemblages that are sufficiently resilient, and which have developmental
Northern Host–Parasite Assemblages     67

tolerances that fall within climatological extremes of temperature and

humidity. Establishment subsequent to colonisation follows from interact-
ing factors that include the temporal limits for natural dispersal, founder
effects, life history and transmission dynamics, generation time, and initial
population density, abundance and spatial distributions (heterogeneous/
homogenous) for hosts and parasites (Hoberg, 2010). Further, there is a
relationship between dispersal ability (vagility) and refugial history (Shafer
et al., 2010; Sandel et al., 2011; Arenas et al., 2012).
Competitive effects may also be a component of structure for these
faunas. Lafferty (2010) commented on microevolutionary phenomena
related to the relative timing and sequential acquisition of pathogens in
the context of mixed infections in individual hosts. In these instances, the
sequence of exposure in multi-pathogen infections was to some degree
a determinant of successful establishment and persistence by respective
pathogens. It is possible that this dynamic also plays out in a macroevo-
lutionary arena where episodic expansion (multiple events of geographic
colonisation) over time could lead to differential infection pressure and
exposures during the development of multi-species assemblages. Com-
petitive interactions by parasites during faunal assembly could conceiv-
ably serve to either limit or facilitate establishment in new geographic
localities, host species and populations over time.
The mode and tempo for biotic expansion further serve to determine
the ultimate structure of complex host–parasite assemblages. Initially
discussed with reference to population biology and genetic diversity as
a legacy of Pleistocene climate cycles (Hewitt, 1996), contrasting mecha-
nisms for expansion can also influence macro-scale structure for parasites
across continents, regions and landscapes (Hoberg, 2005a). Extensive and
slow rates of expansion involving a substantial representation of hosts
and parasites (both species and populations) across geographically broad
fronts (phalanx) may facilitate establishment over time, maintain diversity
in newly established populations and minimise heterogeneity and pat-
terns of peripheral isolation. In contrast, rapid expansion involving small
populations or segments of larger populations (pioneer) may result in
patchy distributions, founder events, local isolation and varying degrees
of diversification or extinction on landscape scales. Historically, indepen-
dent events of parasite dispersal are consistent with pioneer processes
where bottlenecks and peripheral isolation may be prominent. Alternat-
ing or episodic regimes for climate and habitat perturbation during the
Quaternary interact with the mode and tempo for recurrent expansion
(and contraction) events that have differentially influenced parasite faunal
diversity among mammalian hosts (Hewitt, 1996; Hoberg, 2005a).
Various invasion buffers, developmental and behavioural, also influ-
ence the potential outcomes for expansion and establishment of faunal
complexes. Temporal buffers are an intricate interaction of host-centric
68     Eric P. Hoberg et al.

and parasite-centric factors that facilitate continuity of assemblages in

new environmental settings (Hoberg, 2010). Temporal buffers broaden
or extend the time frame under which expansion and introduction may
result in establishment geographically or in new hosts. For example,
extended windows for establishment result from the following: (1) great
host longevity, demographics related to population density and size and
high vagility (e.g. ungulates); (2) recurrent patterns of expansion for host–
parasite assemblages; (3) phalanx dispersal including large numbers on
broad fronts; (4) parasite longevity through indirect cycles over extended
time frames where parasites may be sequestered or live in either defini-
tive or intermediate hosts; (5) parasite longevity in direct cycles where
larvae may exist in arrested stages (e.g. ostertagiines); (6) patterns of inde-
terminate growth and high fecundity (e.g. Umingmakstrongylus); (7) multi-
year life spans (coinciding with host) also leading to high fecundity over
long durations (years) and (8) suitable ecological assemblages or guilds
(Hoberg, 2010; Kutz et al., 2012).
These temporal buffers contrast with factors that result in a limited
or finite window for establishment: (1) limited host longevity, demo-
graphics, low vagility; (2) sporadic or limited expansion; (3) small to
medium mammals and short determinate life spans (e.g. arvicolines,
lagomorphs, mesocarnivores); (4) pioneering expansion involving het-
erogeneity, low numbers, patchy distributions; (5) limited parasite lon-
gevity with determinate life spans, limited fecundity and free-living
stages with limited tolerance and resilience (environmental susceptibil-
ity) (Torchin et al., 2003).
Biotic expansion is further influenced by the presence of environmen-
tal filters that may facilitate or inhibit establishment. Chief among these
were shifts near the Pliocene–Pleistocene boundary (and subsequently in
the Quaternary) between relatively warm to cold and harsh environments
that interacted with tolerances and thresholds for parasite development
and host distribution (e.g. Lister, 2004). Fragmentation of habitats, hetero-
geneity and the distribution of complex and ephemeral refugial zones fur-
ther influenced the potential for persistence of host–parasite assemblages
(Shafer et al., 2010). The directionality of expansion and patterns of diver-
sity in source and recipient regions interact with these filters. Patterns
of absence are attributable in part to biological filters acting on different
components of complex parasite faunas over time. For example, differ-
ential representation of parasite taxa and high-latitude gaps in Holarctic
distributions act as controls on expansion and establishment across Bering
Land Bridge. Alternation of mesic–xeric habitats, which may determine
the distributions for both tundra–steppe floras and an assemblage of mam-
mals (Guthrie, 2001; Galbreath and Cook, 2004; Elias and Crocker, 2008),
would have also directly controlled parasite biogeography. Contemporary
and accelerated climate warming may result in less severe environmental
Northern Host–Parasite Assemblages     69

filters (Callaghan et  al., 2004b) allowing northward expansion of some

parasites and host–parasite assemblages (Hoberg et al., 2008b; Kutz et al.,
2009b; Kutz et al., 2012).

1.5.3. An integrated model for diversification – contributions

from the North
Host switching and geographical dispersal of parasites are common phe-
nomena, occurring on many temporal and spatial scales (Hoberg and
Klassen, 2002; Hoberg, 2005b; Nieberding and Olivieri, 2007; Nieberd-
ing et al., 2008; Hoberg and Brooks, 2008, 2010). Diversification involves
both coevolution and colonisation to explain complex host–parasite
associations. Across the expanse of earth history, the major radiations in
host–parasite assemblages have been preceded by ecological disruption,
ecological breakdown and host switching (Hoberg and Brooks, 2008).
A context for host colonisation is defined by the concept of ecological fit-
ting emerging from phylogenetically conservative capacities for host util-
isation (Janzen, 1985; Brooks and Mclennan, 2002; Agosta and Klemens,
2008; Agosta et al., 2010). Most observed host–parasite associations can be
explained by an historical interaction of taxon pulses (cyclical episodes of
expansion and isolation in geographic range) (Erwin, 1985; Halas et al.,
2005), ecological fitting (defining the potential for events of host colonisa-
tion and initial host range) and oscillation (episodes of increasing host
range alternating with isolation in particular hosts) (Janz and Nylin,
2007). This cyclical process sets the stage for codiversification during peri-
ods of relative stability, punctuated by host switching during episodes of
regional to global environmental disruption and climatological change
(Hoberg and Brooks, 2008, 2010).
Taxon pulses represent repeated episodes of expansion/isolation
occurring in response to climate oscillations. Pulses of expansion result
in episodic and extensive faunal overlap through time and a mosaic
assembly for faunal structure. These signatures contrast with patterns of
synchronic divergence for multiple taxa in response to single or unique
isolation events (=vicariance) (see Halas et al., 2005; Folinsbee and Brooks,
2007). The primary drivers for diversification and faunal assembly irre-
spective of host and parasite taxa are most often associated with several
distinct expansion events in space and time at either intercontinental or
intracontinental scales (Hoberg and Brooks, 2010). Taxon pulses result in
faunal mosaics for parasites structured on varying spatial and temporal
scales and relative to the composition and ecological associations of host
taxa. Vicariance does not result in mosaics.
Major episodes of environmental change appear to be the main drivers
for both persistence and diversification of host–parasite systems, creating
opportunities for host switching during periods of geographic expansion
70     Eric P. Hoberg et al.

and allowing for cospeciation and coadaptation during periods of rela-

tive stasis and geographic isolation (Brooks and Hoberg, 2008; Hoberg
and Brooks, 2008, 2010). The patterns and dynamics of contemporary
host–parasite associations emerge from an evolutionary context in which
geographic distributions and environment play a key role (e.g. Vrba,
1985) and represent a manifestation of the general evolutionary model
for the ‘sloshing bucket’ where ecological perturbation represents a pri-
mary driver for diversification (Eldredge, 2008; Brooks and Hoberg, 2008;
Hoberg and Brooks, 2008). Hierarchical scale and extent (magnitude) of
perturbation may be critical factors in determining outcomes for biotic
systems and a continuum linking diversification, turnover and extinc-
tion. Much of what we observe today in northern systems is a legacy of
a tumultuous evolutionary history emerging from ecological perturba-
tion at varying spatiotemporal scales. The Arctic represents a particularly
powerful and tractable exemplar system for exploring these interacting
The generality for taxon pulses as drivers or determinants of faunal
structure in shallow evolutionary and ecological time is revealed in the
Beringian region. Initially, this nexus for Eurasian and Nearctic faunas
was emergent through much of the Tertiary, serving as a primary path-
way for interchange of terrestrial faunas during times of relatively equi-
table climate culminating in the Pliocene. As a crossroads for the northern
continents, Beringia strongly influenced patterns of distribution and
speciation, alternately serving as a barrier or pathway for expansion of
marine and terrestrial faunas and as a centre for diversification over the
past 4–5 Myr (Hopkins, 1959; Sher, 1999). The episodic nature of intersta-
dial–stadial cycles, numbering 20 events during the late Pliocene/Quater-
nary, together with patterns of biotic expansion and isolation at inter- and
intracontinental scales and formation/dissolution of intermittent refugia
have had pervasive effects on the history (speciation, extinction) and dis-
tribution of a complex mosaic of host–parasite systems from the Holarctic
to the Neotropics (e.g. Rausch, 1994; Hoberg et al., 2003; Hoberg, 2005a;
Cook et al., 2005; Dragoo et al., 2006; Zarlenga et al., 2006; Koehler et al.,
2009; Pozio et al., 2009) (Fig. 1.4).

1.5.4. Mosaic faunas – consequences of episodic

geographic expansion
The dynamics of taxon pulses or recurrent patterns of geographic
expansion and isolation in conjunction with episodic host colonisation
results in a mosaic structure for parasite faunas. Geographic expansion
and host colonisation appear to be pervasive mechanisms in driving the
structure of host and parasites associations (Hoberg and Klassen, 2002;
Hoberg and Brooks, 2008, 2010) and have been identified as important
Northern Host–Parasite Assemblages     71

macroevolutionary determinants for patterns of diversity in northern

Mosaics were originally discussed in the context of invasion biology
related to faunal (regional – interspecific) or populational (landscape –
intraspecific) admixtures of endemic and introduced species brought into
contact and sympatry by anthropogenic translocation and introduction
(e.g. Hoberg et  al., 1999, 2008b; Hoberg, 2005a, 2010). Mosaic structure,
however, is a fundamental phenomenon, an observation that emerges
from the idea that processes serving as determinants of complex parasite
faunas are equivalent in evolutionary and ecological time (Hoberg and
Brooks, 2008, 2010). A conceptual linkage to the original terminology for
coevolutionary mosaics as established by Thompson (2005) is also evi-
dent. Mosaics are further consistent with the sloshing bucket model of
evolution with respect to the diversification and maintenance of intricate
faunal assemblages linking ecological and evolutionary hierarchies (e.g.
Eldredge, 2008; Brooks and Hoberg, 2008).
Faunal mosaic structure results from recurrent biotic expansion that
drives the potential for geographic colonisation by hosts and parasites
and possibly secondary host colonisation over extended time frames.
Consider the timing of expansion, arrival and establishment for dispa-
rate elements of a fauna within the context of host ecology and bioge-
ography (sympatry, temporally and spatially, is necessary as a driver of
switching). Trophic linkages, food webs and guilds in conjunction with
ecological fitting establish the potential for switching (e.g. Hoberg and
Adams, 2000; Brooks and Hoberg, 2008). Switching is maximised among
ecologically similar assemblages in proximity or contact and where host
resources (for parasites) are plesiomorphic. Notably, these patterns are
exemplified for Taenia, Trichinella and Soboliphyme among terrestrial car-
nivores (e.g. Hoberg, 2006; Zarlenga et al., 2006; Koehler et al., 2007, 2009;
Pozio et  al., 2009); tetrabothriid tapeworms among pinnipeds (Hoberg
and Adams, 2000); nematodirines and protostrongylids among ungulates
(Hoberg et al., 2002b; Hoberg, 2005a); nematodirines and heligmosomes
among lagomorphs (Hoberg, 2005a; Durette-Desset et al., 2010) and anop-
locephalines in rodents and lagomorphs (Haukisalmi et  al., 2001, 2006,
2009; Wickström et al., 2005). Defining mosaic structure in space and time

Mosaic structure constitutes a continuum resulting from large-scale
(regions and faunas) to fine scale (landscapes and populations) processes
acting on the distribution of diversity. Consequently, mosaics are mani-
fested spatially and temporally and can involve multi-taxon and interspe-
cific associations in addition to intraspecific and populational interactions
(Hoberg et  al., 1999, 2008b; Hoberg, 2010). Mosaics result from faunal
72     Eric P. Hoberg et al.

interchange and invasion, both general phenomena in evolutionary and

ecological time (e.g. Marshall et  al., 1982; Vermeij, 1991; Hoberg and
Brooks, 2010; Hoberg, 2010).
Faunal and regional mosaics may result from expansion over one-time
land connections, as exemplified in South America with the emergence of
the Panamanian Isthmus that involved complex assemblages of mamma-
lian taxa beginning about 3Ma (Marshall et al., 1982). Unique or one-time
events contrast with episodic processes that bring faunas, congeneric spe-
cies or populations into recurrent contact on varying temporal and spa-
tial scales, as demonstrated in Beringia and the amphiberingian region
over the past 3–5Ma. These latter exchanges ultimately served as determi-
nants of contemporary biotic structure in assemblages of mammals and
parasites of the Holarctic and downstream into the Neotropical zone (e.g.
Hoberg 2005a; Pozio et al., 2009). On northern regional scales, postglacial
expansion out of refugial centres leading to secondary contact or colonisa-
tion also is a driver of mosaic structure (Shafer et al., 2010; Galbreath and
Hoberg, 2012; Hoberg et al., in press-a). Within this general framework,
several classes of mosaics can be defined.
Macroevolutionary faunal mosaics. These are temporal mosaics (ver-
tical or chronological) representing disparate assembly correlated with dif-
ferential expansion and establishment over time. Discrete episodes (taxon
pulses) for host expansion/colonisation lead to historical mosaics com-
posed of elements representing associations and faunas of disparate age.
Episodes involving taxon pulses influence the arrival times for diverse
assemblages representing different taxonomic groups and multiple spe-
cies. Vertical mosaics contribute to the large patterns for diversity and
faunal structure (intercontinental, continental, regional) in the context of
environmental and biotic filters and constraints. These faunal associations
involve species diversity and mechanisms that emphasise interspecific
variation and sympatry. Examples are in the occurrence of assemblages
composed of species groups of disparate age across particular host groups.
Hierarchies are of disparate ages and phylogenetically diverse (consider
comparisons for ungulates, arvicolines or Ochotona) where specific struc-
ture for particular host–parasite assemblages is nested within larger fau-
nal associations. Mosaics contrast with mechanisms derived from simple
vicariance (e.g. Hoberg and Brooks, 2008, 2010) where all elements of a
fauna undergoing simultaneous, large-scale and permanent isolation
would be predicted to be of equivalent age. That such mosaics appear to
be common suggests that vicariance may not always have strong explana-
tory power (Hoberg and Brooks, 2008, 2010).
Horizontal or geospatial mosaics. Spatial mosaics nest within
temporal associations reflecting patterns of assembly correlated with
geography and the geographic extent of expansion or invasion. Refu-
gial effects are emphasised as are primary and secondary patterns
Northern Host–Parasite Assemblages     73

of geographic colonisation as a manifestation of taxon pulses. These

mosaics denote persistent or recurrent refugia in space and time that
is a generality for late Pleistocene environments across the circumpo-
lar region, but of particular significance in trans-Beringian faunas and
in the Nearctic (Galbreath, 2009; Shafer et  al., 2010). Related to this is
the concept of habitat heterogeneity and ‘refugia within refugia’ during
particular glacial stages (e.g. Shafer et al., 2010, 2011).
Microevolutionary population mosaics. Landscape scale mosaics
involving populations, emergent from deeper historical processes and asso-
ciations, are manifested by spatial heterogeneity at the intraspecific level
that may be ephemeral in space and time (Thompson, 2005). Population
mosaics are hierarchical and nested within larger temporal and horizontal
structure for host–parasite assemblages. At a microevolutionary scale, these
associations reflect local phenomena and represent the potential for recipro-
cal coadaptation (a microevolutionary counterpart of cospeciation that is not
generally a driver of diversification) and may be tied to transient outbreaks
of disease on landscape scales (Hoberg and Brooks, 2010; Hoberg, 2010).
Anthropogenic invasion mosaics. These mosaics represent the out-
come of processes in ecological time where admixtures of endemic and
introduced species (or populations) result from human-mediated trans-
location and introduction of otherwise non-indigenous taxa (Hoberg,
2010). Such mechanisms not only can influence faunal diversity across
regions but also may extend to the population level on landscape scales
(Thompson, 2005). Primary examples emerge from the interface for natu-
ral and managed systems and are most evident among nematode para-
site assemblages in ungulates (Hoberg et al., 1999, 2008b; Hoberg 2010).
In instances where translocation is used to reintroduce host populations,
as has occurred for some mesocarnivores and ungulates, there is also the
potential for development of mosaics that may have implications in con-
servation biology (Hoberg et al., in press-b).
Contemporary invasion mosaics. Invasions played out in ecological
time may reflect accelerated expansion resulting in rapid and changing
patterns of distribution for host–parasite assemblages. Invasion mosa-
ics involving faunas, species or populations may result from shifts in
distribution mediated by accelerated climate warming and habitat per-
turbation (Parmesan, 2006; Post et al., 2009; Lawler et al., 2009) with the
development of new ecotones and patterns of infection. For example,
substantial northward expansion is projected for assemblages of nema-
tode parasites in ungulates, bringing temperate and high-latitude faunas
into contact (Hoberg et  al., 2008a,b; Kutz et  al., 2009b; De Bruyn, 2010;
Kutz et al., 2012).
Outcomes for faunal mixing, which apply generally in evolutionary
and ecological time, include (1) faunas that remain discrete in respec-
tive endemic and newly arrived hosts; (2) parasite species that remain
74     Eric P. Hoberg et al.

discrete, but faunal structure reflects reciprocal exchange (or unidirec-

tional host colonisation) often at ecotones; (3) hybridisation or introgres-
sion and (4) displacement of an endemic fauna. Processes may be played
out over extended spatiotemporal scales from primary intercontinental
events to regions and landscapes in ecological time and in instances of
postglacial expansion from refugial centres and development of second-
ary contact zones for hosts and parasites. Our developing understanding
of the historical origins and complex structure for mosaics is essential in
formulating predictions about responses to environmental perturbation in
northern systems.

1.5.5. Stories that parasites reveal

Phylogenetics has become the foundation for exploring complex associa-
tions and patterns of diversification, providing a pathway and context
for discovery (e.g. Brooks, 1979, 1981; Brooks and McLennan, 2002; Page,
2003; Hoberg 2005b; Hoberg and Brooks, 2008; Nieberding et  al., 2008).
Hierarchical order reveals historical relationships and most critically con-
strains the range of explanations for the structure, biogeography and his-
torical ecology of complex host–parasite systems (Hoberg, 1997a, 2005b);
inference emerges from complex data sets combining morphological and
molecular attributes. Phylogenies are the tapestry to elucidate interactions
related to speciation processes, coevolution, colonisation and extinction,
faunal structure and the environment and ecological continuity across
temporal and biogeographic scales.
The past century has been dominated by coevolutionary thinking
with respect to questions about diversity and faunal structure. Processes
for diversification were most often linked to cospeciation and asso-
ciation by descent between host and parasite lineages (summarised in
Klassen, 1992; Brooks and McLennan, 1993, 2002; Paterson and Banks,
2001; Page, 2003). Extensions of this paradigm for ‘maximum cospecia-
tion’ included formalised assumptions about the evolutionary similarity
of parasite species in phylogenetically related hosts. Thus, faunas should
be of relatively uniform age with respect to the host groups that they
inhabit, and single species were often considered to be geographically
widespread. Following from these observations, common parasite spe-
cies should also occur in both domestic and free-ranging hosts as an
evolutionary legacy of diversification. For example, this was reflected
in concepts for the apparently widespread distributions of nematode
species in broad arrays of ungulate hosts but is also more generally
applicable (e.g. Hoberg et al., 1999).
The coevolutionary reality, however, was discovered to be rather dif-
ferent and considerably more intricate (e.g. Hoberg and Klassen, 2002)
with the idea of pervasive cospeciation giving way to a mechanistically
Northern Host–Parasite Assemblages     75

complex picture of diversification often driven by host and geographic

colonisation on varying spatial and temporal scales linking evolutionary
and ecological time (e.g. Hoberg and Brooks, 2008, 2010). The number of
studies demonstrating a prominent signal of cospeciation in helminth
parasite systems is vanishingly small and these often involve microevo-
lutionary processes of coadaptation rather than macroevolutionary driv-
ers for diversification over time (Nieberding et al., 2008). This observation
is increasingly consistent with diverse assemblages that have so far been
explored in northern systems and globally. Examples of cospeciation are
the exception and where such associations are identified, these are most
often nested within hierarchies originally established through processes
for colonisation (e.g. Wickström et al., 2005; Haukisalmi et al., 2010). Fur-
ther, corroboration of the rarity of association by descent as a driver for
speciation emerges and concurrently identifies processes of colonisation
as substantial contributors to diversification on varying scales (Hoberg
and Klassen, 2002; Hoberg and Brooks 2008, 2010).
In northern systems, colonisation processes are particularly evident
among unrelated mammalian groups – e.g. soricomorphs and arvicolines
in diversification of hymenolepedids (Haukisalmi et al. 2010), or among
particular host groups such as arvicolines with diversification of Paranop-
locephala and Anoplocephaloides (e.g. Haukisalmi et al., 2009). Colonisation
has been the precursor for major radiations by parasite groups in diverse
host taxa and has influenced species-level diversification within nearly all
helminth groups that have been explored (e.g. Hoberg and Brooks, 2008).
Further, there are very few widespread species of parasites and consid-
erably greater diversity in many helminth taxa than previously consid-
ered. For example, the Holarctic tapeworm, Arostrilepis horrida, has now
been demonstrated to represent over 13 species-level lineages distributed
among species of cricetid rodents from Eurasia and North America (Cook
et al., 2005; Makarikov et al., in press). Additionally, considerable diver-
sity is now recognised among anoplocephaline tapeworms where mul-
tiple species complexes have been demonstrated (Haukisalmi et al., 2004,
2008, 2009). Although specificity is often apparent in these assemblages,
diversification was driven to some degree by colonisation events of vari-
ous host taxa.
Parasites reveal a nuanced history for the structure and diversity of
faunal assemblages (Hoberg, 1995, 1997a; Hoberg and Brooks, 2008;
­Koehler et al., 2009; Nieberding and Olivieri, 2007; Nieberding et al., 2008;
Hoberg et al., in press-a). Concerted or synchronic expansion and isolation
may result in general patterns of distribution and broad regional struc-
ture as exemplified by vicariance among single or multiple taxa linked
to unique events. In contrast, asynchronous expansion leads to idiosyn-
cratic patterns established at regional to local scales for multiple taxa over
extended time frames (Hoberg and Brooks, 2010). These patterns reflect
76     Eric P. Hoberg et al.

episodic processes and responses to differential gradients, habitat and

biotic filters that are unlikely to be temporally uniform but are event spe-
cific in space and time. Dispersal or expansion has been a primary initiator
for biotic structure played out in a dynamic environment of change and a
physical mosaic of heterogeneous habitats (Guthrie, 2001, 2006). Processes
in Beringia and northern systems in general emphasise the importance
of ephemeral associations for host and parasite taxa. In these situations,
parasites may reveal transient historical zones of contact for host species
or populations that otherwise remain cryptic and not immediately identi-
fied (e.g. Hoberg, 1995; Koehler et al., 2009; Galbreath and Hoberg, 2012).
Although we regard episodic dispersal/isolation as a defining process
for the northern fauna, the degree to which expansion events (within a
specific time frame) are synchronous across all groups of mammalian taxa
is unknown. For example, Repenning (2001) suggested that geographic
expansion (across Beringia from the Palaearctic) among arvicoline rodents
was confined to periods early in major glacial cycles and then later dur-
ing the peaks of minor glacial advances (stadials) as a function of habitat
structure and temperature. This may contrast with either ungulates or
carnivores that may not have been as strongly limited by habitat require-
ments and would be expected to have greater vagility.
Current diversity in northern systems represents the outcome of inter-
actions of biotic and abiotic factors that have unfolded in a complex geo-
graphic arena since the Pliocene. Biogeographic and phylogeographic
inference has identified multiple sources for faunal assemblages, under
the influence of recurrent expansion events from Eurasia, and regional
to local effects involving local extinctions and patterns of repopulation.
Both geographic colonisation and in situ speciation have contributed to
the structure and diversity of the northern fauna. In the Nearctic, an inter-
play of processes through the Quaternary in association with Beringian
environments has facilitated both diversification and dissemination of a
speciose and complex parasite fauna linked to mammalian hosts (Rausch,
1994; Cook et al., 2005; Waltari et al., 2007b). Faunal structure represents
the accumulation of species over time and development of spatial and
temporal mosaics resulting from episodes of biotic expansion involving
phylogenetically disparate or homologous assemblages.


Explorations of parasite faunal diversity in northern systems and other

regions of the globe are dependent on the availability of sophisticated
tools and resources for biodiversity informatics (Table 1.8). Although
methodological approaches in phylogeography and biogeography have
grown increasingly robust (Avise, 2000; Nieberding et al., 2008; Galbreath
Northern Host–Parasite Assemblages     77

TABLE 1.8  Field-based and analytical tools for the discovery of biodiversity in
northern host–parasite systems

Definitions of parasite diversity

• Geographically extensive and site intensive sampling/ecosystem-level
• Integrative species-level identifications with morphological and molecular
• Species concepts linked to phylogeny and hypothesis testing
• Explorations of cryptic diversity among species
• Phylogeography and population-level approaches
• Molecular-based prospecting for diversity
• Patterns of host and geographic associations on regional to landscape scales
• Genealogical, ecological and numerical diversity

Articulation of historical baselines

• Archival, specimen-based museum resources for morphology and
• Informatics resources for the distribution of diversity linked to collections
• Host–parasite phylogenetic frameworks
• Historical ecology, biogeography/phylogeography to define abiotic and
biotic components of faunal structure and assembly
• Definition of abiotic and biotic drivers of distribution/diversification in
­evolutionary/ecological time

Linkage to contemporary systems

• Geographic information system applications
• Geographic modelling (e.g. ecological niche modelling) to explore
­determinants of distribution over time
• Environmental effects and constraints on distribution
○ Thresholds/developmental rates/environmental resilience and
• Historical analogues for prediction of change in complex systems
○ Responses related to climate and habitat perturbation
○ Invasion biology in evolutionary and ecological time
• Surveillance networks and monitoring

and Hoberg, 2012), we are still fundamentally limited by the quality, scope
and depth of archival biological collections that document patterns of
diversity. Specimens remain the most critical self-correcting records for
biodiversity and in conjunction with baselines from survey and inven-
tory give us a glimpse of faunal structure within particular time frames
(e.g. Hoberg et al., 2003; Hoberg et al., 2009; Kutz et al., 2012). Biodiversity
baselines that combine specimen-based records with informatics about
78     Eric P. Hoberg et al.

geographic distribution and host associations are fundamental to tracking

complex host–parasite systems in space and time. Archival resources are
the synergistic tools that link synoptic and strategic field collections with
informatics emanating from phylogenies, history, biogeography, ecology
and population structure. Modern biodiversity assessment is integrative
and relies on the unification of methods and interpretations derived from
molecular and morphologically based approaches (Brooks and Hoberg,
2000, 2006; Cook et al., 2005; Criscione et al., 2005; Koehler et al., 2009).
Archives and biodiversity baselines become the primary tools for
understanding the structure of the biosphere (Brooks and Hoberg,
2000; Hoberg, 2002; Hoberg et al., 2003; Cook et al., 2005; Hoberg et al.,
2008a,b, 2009). The need for integrated approaches combining compara-
tive morphology remains as a foundation or anchor for determination
of morphospecies and combined with phylogeography and population
genetics provides recognition of occurrence of cryptic species and species
complexes (Criscione et al., 2005; Kutz et al., 2007; Pérez-Ponce de León
and Nadler, 2010). Further, site-intensive and geographically extensive
sampling with a shift to application of molecular epizootiological probes,
which to some extent replace laborious necropsy procedures, can greatly
facilitate our capacity for monitoring and tracking changes in geographic
ranges, patterns of host associations and transmission (Hoberg et al., 2001;
Jenkins et al., 2005; Kutz et al., 2007; Asmundsson et al., 2008). By exten-
sion, there is a need to explore population genetics/phylogeography as
a basis to identify geographic sources for faunas, histories for natural
expansion, historical introductions and interactions at ecotones (Koehler
et al., 2009; Hoberg et al., in press-a).
Our current understanding of the general patterns of parasite biodi-
versity in northern systems is emerging from large-scale or synoptic bio-
logical collections linked to assessments of ecology, biogeography and
phylogeography in some regional settings such as Beringia (e.g. Hoberg
et al., 2003; Cook et al., 2005). Additionally, during the International Polar
Year, a broad-based and standardised project exploring health of reindeer
and caribou was initiated under the CircumArctic Rangifer Monitoring
and Assessment Network (Kutz et al., in press). Similar inventories, how-
ever, are underrepresented across Arctic latitudes. Essentially, there are
few comprehensive historical baselines (derived from comparable sam-
pling standards) against which to measure trends for changing patterns
of distribution, host associations or prevalence and abundance of most
parasites (and diseases) in free-ranging and domestic animals or in people
in a regime of accelerated climate change. Indeed, we continue to have an
unbalanced or incomplete picture of diversity, host associations and distri-
bution for parasites in vertebrates and invertebrates in northern regions.
Collections establish the linkage between historical process in evolution-
ary and ecological time (Hoberg et al., 2009).
Northern Host–Parasite Assemblages     79

Systematics also remains as a primary cornerstone. Specimens, associ-

ated data and permanent collections provide a solid foundation for sys-
tematics research through creation of an empirical record that validates
our understanding of the biosphere. The specimen-linked record, how-
ever, is patchy, and despite an extensive published record derived from
survey and inventory (e.g. Rausch, 1952; Gvozdev et al., 1970; Boev, 1975;
Priadko, 1976; Ryzhikov et al., 1979; Govorka et al., 1988; Rausch, 1994),
relatively few vouchers from field collections of terrestrial mammals
now exist in major museum collections in North America or Eurasia. The
importance of having access to well-documented and representative col-
lections of great geographic scope and taxonomic depth is readily appar-
ent (Hoberg et al., 2009).


A century or more of focused investigations in the North leaves many

unresolved questions that are critical for understanding the outcomes
of environmental change and socioeconomic forcing in these systems.
Considerable unknown diversity remains to be discovered. We have
highlighted this through a number of new genera and species complexes
discovered among ungulates over the past decade (e.g. Umingmakstron-
gylus pallikuukensis, Teladorsagia boreoarcticus and species of Marshallagia
and Varestrongylus) as well as recognition of new or expanded geo-
graphic ranges or host associations for parasites (Parelaphostrongylus
odocoilei, Protostrongylus stilesi). Considerable diversity has also been
discovered among the parasites of arvicoline rodents (e.g. species of
Paranoplocephala and Anoplocephaloides along with new assemblages of
genera and species of Arostrilepis). Further, a unified picture of dynamic
and episodic expansion as the driver for patterns of diversity is now
well established.
There are consequences to unknown diversity, particularly evident
in the potential for emerging diseases and the interface of this phenom-
enon with rapid climate change and environmental perturbation (e.g.
Brooks and Hoberg, 2006, 2007; Hoberg et al., 2008a, 2008b; Kutz et al.,
2009b, 2012). In this regard, we continue to have minimal information for
a number of potential helminth pathogens among ungulates including
filarioids such as Setaria, Rumenfilaria and Onchocerca, lungworms such
as Dictyocaulus and gastrointestinal nematodes including an array of
ostertagiines and nematodirines (Kutz et al., 2012). In some cases where
we have established the limits for diversity among morphospecies of
zoonotic pathogens such as Echinococcus and Trichinella, distributions
and genetic structure remain to be resolved (Rausch, 1967; Thompson
et al., 2005; Nakao et al., 2009).
80     Eric P. Hoberg et al.

The importance of understanding northern systems is indicated by

their value as historical models to recognise and define processes involved
in faunal assembly and biodiversity (Waltari et al., 2007a,b; Waltari and
Perkins, 2010; Galbreath and Hoberg, 2012). In northern systems and adja-
cent regions, dispersal, episodic geographic colonisation, host switching,
range fragmentation and isolation of host–parasite populations at inter-
and intracontinental scales have been universal drivers for diversification
through the late Tertiary and Quaternary. Our ability to explore historical
responses to episodic shifts in global climate provides a window or ana-
logue for predicting the cascading effects of rapid environmental change
in contemporary systems. Historically, invasive faunas characterise the
Arctic, and processes of invasion and colonisation, both primary and sec-
ondary effects, have been substantial drivers. We have the opportunity to
reveal microevolutionary phenomena played out on a macroevolutionary
landscape that creates the backbone for faunal structure.
Pervasive host colonisation historically is the precursor that sets the
stage for host switching driven by contemporary ecological perturbation
and predicts major changes in current high-latitude systems. The maps
will be redrawn for many complex host–parasite assemblages over the
coming century. We can use history to define links across Quaternary,
contemporary and future systems and climate states where equivalent
processes have been in play and will continue to be forces that shape eco-
systems and faunas:
• Development of novel and transitional environments, rapid change
• Changing geographical distributions for environments
• Rapid changes in faunal distributions
• Development of secondary contact zones and/or new associations for
host groups
• Accelerated host switching
• Mosaic faunal structure
• Mosaic patterns for ephemeral emergence of diseases in space and
As we have discussed in detail elsewhere, the issue of emergent and inva-
sive pathogens represents a component of the biodiversity crisis linked to
an absence of a comprehensive global taxonomic inventory for parasites
(Brooks and Hoberg, 2006). On broad global scales, there are cascading or
attendant threats to natural systems, human populations, conservation,
agriculture and the global economy. Continuity for ecological and evo-
lutionary mechanisms is universal and emphasises associations for pro-
cesses (biotic expansion, translocation, faunal disruption, establishment,
host switching) and outcomes (faunal structure, emergence of diseases).
Incorporation of historical mechanisms to understanding past and current
faunal structure signals a need to shift from a response-based stance rela-
tive to emerging diseases to a discovery (prediction) -based stance (Brooks
Northern Host–Parasite Assemblages     81

and Hoberg, 2007; Hoberg and Brooks, 2008, 2010; Agosta et al., 2010). The
Arctic is but one piece of a larger interconnected global puzzle.
The Arctic, an obscure place beyond the far horizon for most people, has
also held the imagination of many as an extreme and challenging environ-
ment where highly adapted societies have lived for millennia, but where
European and western exploration seldom ventured until the last 200–300
years (e.g. Lopez, 1986; Berton, 1988; Krupnick, 1993). Faunal diversity in
the North represents interactions at a complex interface linking natural pro-
cesses in evolutionary time with events that have unfolded in ecological time
since the earliest human occupation of high-latitude systems. Consequently,
people are an integral part of the equation for understanding the past and
present and in determining a pathway to the future for these fragile biotas.

Our exploration of diversity builds on a rich history of research dealing with the northern
fauna and the processes that serve to structure complex biological systems. We are indebted
to Robert L. Rausch and Virginia R. Rausch for their friendship, insights and guidance over
many years of our work in Alaska, the Canadian Arctic and Siberia. David M. Hopkins served
as a critical mentor for E.P.H. and J.A.C. in all things Beringian and introduced us to an intri-
cate historical picture for the north. Appreciation is extended to Vytus Kontrimavichus and
Svetlana Bondarenko who provided a gateway to Chukhotka through the Institute for Bio-
logical Problems of the North in Magadan during the early 1980s. Steven O. MacDonald has
made a huge impact on our integrated field expeditions, as have a large number of Russian
collaborators. A decade of field studies and collaborations with Heikki Henttonen, Voitto
Haukisalmi and Lotta Hardman (Wickström) of the Vantaa Forest Research Center contrib-
uted substantially to our understanding of high-latitude diversity. Further, we thank Alas-
dair Veitch, Richard Popko and Brett Elkin of the Government of the Northwest Territories
(GNT) at Norman Wells and Yellowknife, NT, for their critical contributions to mammalian
parasitology and the opportunity to have interesting experiences in small fixed wing air-
craft on the borders of the Arctic Circle. Our original work in the central Canadian Arctic on
ungulate parasites was greatly facilitated by John Nishi, formerly of the GNT at Coppermine
(now Kugluktuk, Nunavut). Lastly, this view of the biosphere and synergy of geo-expansion,
episodic events and invasion biology was catalysed over the past decade through discussions
and collaborations with Daniel R. Brooks, now at the University of Nebraska-Lincoln. This is
a contribution of the Beringian Coevolution Project, a multi-national research collaboration to
explore diversity across the roof of the world, supported by grants from the National Science
Foundation (DEB 0196095 and 0415668) to J.A.C. at the Museum of Southwestern Biology,
University of New Mexico, and E.P.H. at the US National Parasite Collection.

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Parasites in Ungulates of Arctic
North America and Greenland:
A View of Contemporary
Diversity, Ecology, and Impact
in a World Under Change
Susan J. Kutz*, Julie Ducrocq*, Guilherme G.
Verocai*, Bryanne M. Hoar*, Doug D. Colwell†,
Kimberlee B. Beckmen‡, Lydden Polley§,
Brett T. Elkin¶, and Eric P. Hoberg^

Contents 2.1. Introduction 101

2.1.1. The Arctic 101
2.1.2. Parasites in a changing Arctic 102
2.2. Arctic Ungulate Hosts 103
2.2.1. Caribou – Rangifer tarandus ssp. 103
2.2.2. Muskoxen – Ovibos moschatus ssp. 107
2.2.3. Moose – Alces americanus ssp. 108
2.2.4. Dall’s Sheep – Ovis dalli dalli 112
2.2.5. Other ungulate hosts 113

*  University of Calgary, Faculty of Veterinary Medicine, Calgary, Alberta, Canada,

†  Agriculture and Agri-food Canada, Lethbridge, Alberta, Canada,

 Alaska Department of Fish and Game, Division of Wildlife Conservation, Fairbanks, AK, United
 University of Saskatchewan, Western College of Veterinary Medicine, Saskatoon, Saskatchewan,

 Environment and Natural Resources, Government of Northwest Territories, Yellowknife, Northwest
Territories, Canada,
^ US National Parasite Collection, Animal Parasitic Diseases Laboratory, Agricultural Research Service,

USDA, Beltsville, MD, USA

Advances in Parasitology, Volume 79 © 2012 Elsevier Ltd.

ISSN 0091-679X, All rights reserved.

100     Susan J. Kutz et al.

2.3. Nematodes 113

2.3.1. Nematodes of the gastrointestinal tract 113
2.3.2. Lung and tissue nematodes: Protostrongylidae
and Dictyocaulinae 139
2.3.3. Other tissue nematodes: Onchocercidae 160
2.4. Cestodes 165
2.4.1. Ungulates as Intermediate hosts: Taeniidae 165
2.4.2. Ungulates as definitive hosts: Anoplocephalidae 171
2.4.3. Emerging issues and knowledge gaps
for the Cestoda 173
2.5. Trematodes 173
2.5.1. Family Fasciolidae 174
2.5.2. Family Paramphistomidae 176
2.6. Protozoa 177
2.6.1. Protozoa of the gastrointestinal tract 177
2.6.2. Tissue and blood protozoa: the Sarcocystidae,
Trypansomatidae and Babesiidae 183
2.7. Arthropods 198
2.7.1. Diptera 200
2.7.2. Phthiraptera 204
2.7.3. Acari 207
2.7.4. Crustacea, Pentastomida 209
2.7.5. Emerging issues and future research
for the Arthropoda 210
2.8. Discussion 210
2.8.1. Parasites alive and well in arctic ungulates 210
2.8.2. Parasite biodiversity 211
2.8.3. Characteristics of arctic parasites: New insights 212
2.8.4. Exploring characteristics of arctic
parasites in a broader framework 217
2.8.5. Changing polar environments and host–parasite
interactions 218
2.8.6. Directions forward 220
2.8.7. Conclusions 223
Acknowledgements 224
References 225

Abstract Parasites play an important role in the structure and function of

arctic ecosystems, systems that are currently experiencing an un-
precedented rate of change due to various anthropogenic pertur-
bations, including climate change. Ungulates such as muskoxen,
caribou, moose and Dall’s sheep are also important components of
northern ecosystems and are a source of food and income, as well
as a focus for maintenance of cultural traditions, for northerners.
Parasites of ungulates can influence host health, population dynam-
ics and the quality, quantity and safety of meat and other products
of animal origin consumed by people. In this article, we provide a
Parasites in Ungulates of Arctic North America and Greenland     101

contemporary view of the diversity of nematode, cestode, trema-

tode, protozoan and arthropod parasites of ungulates in arctic and
subarctic North America and Greenland. We explore the intricate
associations among host and parasite assemblages and identify key
issues and gaps in knowledge that emerge in a regime of accelerating
environmental transition.

List of acronyms
State or province or Country
AK Alaska (state of the USA)
GL Greenland
NL Newfoundland/Labrador
NT Northwest Territories (territory of Canada)
QC Québec (province of Canada)
NU Nunavut Territory (territory of Canada)
YT Yukon Territory (territory of Canada)


2.1.1. The Arctic

The Earth’s northern circumpolar regions present landscapes of stunning
natural beauty – windswept tundra in the north, boreal coniferous forests
to the south, mountains, glaciers and ice sheets. Small, isolated settlements
are scattered throughout and are inhabited by people of great resilience
who maintain close ties to the land. The northern climate is extreme – long
cold winters, short cool summers and, at higher latitudes, months of con-
tinuous darkness in winter and of continuous sunlight in summer. These
regions also support a unique fauna and flora and provide many valuable
non-renewable resources for the world.
In the Nearctic, Alaska (AK), Yukon (YT), Northwest Territories (NT),
Nunavut (NU) and Greenland occupy almost eight million square kilome-
tres of the Earth’s surface (almost sixteen times the size of France), yet they
are home to less than one million people. Approximately three quarters of
these northern people live in Alaska and one quarter of the total popula-
tion are aboriginal, with Greenland (88%) and Nunavut (84%) having the
highest, and Alaska (15%) the lowest, proportions.
For many northerners, especially aboriginal peoples, wildlife (mam-
mals, birds and fish) are important sources of food through subsistence
hunting, generate economic activity through sport hunting and tour-
ism and are vital for the maintenance of many cultural traditions. For
example, in the NT, approximately 40% of the residents aged 15 years
and above hunted or fished during 2008 and in almost 30% of house-
102     Susan J. Kutz et al.

holds >50% of the food consumed had been acquired by hunting or fish-
ing (Anonymous, 2009).
This circumpolar ecosystem has been shaped over time by a variety of
complex biotic and abiotic processes. It continues to undergo significant,
and in some instances, accelerating change, much of which results from
human activity, both local and distant, and which has the potential for
global impact (IPCC, 2007).

2.1.2. Parasites in a changing Arctic

Parasites are important components of the arctic ecosystem, influencing
health and sustainability of wildlife populations and the health and well-
being of the people who depend on wildlife. Beginning in the 1940s, a succes-
sion of parasitologists and ecologists have explored parasitism in the Arctic
and advanced understanding of the structure and function of northern host–
parasite systems (Rausch, 1974; Hoberg et al., 2012). In recent years, the rec-
ognition of rapid change in the North has increased these efforts.
Accelerated climate warming and perhaps other anthropogenic land-
scape perturbations are having measurable biological impacts on the
Arctic, including the ecology of ungulates and host–parasite interactions
(IPCC, 2007; Kutz et  al., 2009a; Post et  al., 2009). Ungulates are impor-
tant components of any ecosystem, serving as food for various carnivores,
omnivores and scavengers. They also influence the abundance and diver-
sity of vegetation and affect soil quality (Danell et al., 2002; Bruun et al.,
2008). In the Arctic, ungulates are important sources of food and income
as well as a focus of traditional activities for indigenous peoples (AMAP,
2002; Nancarrow and Chan, 2010). Additionally, they provide an impor-
tant habitat for various helminth, protozoan and arthropod parasites
(Hoberg et al., 2008a; Kutz et al., 2009b).
Parasites can cause significant clinical and subclinical disease in wild-
life and consequently influence the dynamics and trajectory of wildlife
populations (Hudson and Dobson, 1997; Hudson and Greenman, 1998;
Irvine et al., 2000). The biodiversity, abundance and impacts of macro and
micro parasites in arctic wildlife are highly sensitive to climate and cli-
mate change as well as to other anthropogenic disturbances at the land-
scape level (Kutz et al., 2009a,b; Laaksonen et al., 2010a). The current rate
of climate and landscape change in the Arctic is expected to alter host–
parasite interactions and is a significant concern for the sustainability of
arctic ungulates (Hoberg et al., 2008b; Kutz et al., 2009a; Polley et al., 2010).
In addition to direct effects on host populations, changes in parasitism
in wildlife can also have significant impacts on the people who depend
on wildlife. Parasites can affect the quality, quantity and safety of meat
and other products of animal origin consumed by people and changes in
parasite biodiversity and/or in associated disease processes can ­influence
Parasites in Ungulates of Arctic North America and Greenland     103

nutrition, activity levels and the sustainability of cultural activities for

northern aboriginal peoples (Davidson et al., 2011).
Although parasitism is often portrayed as a negative process, parasites
play important roles and provide unique insights into the historical and
current status and health of ecosystems. They reflect trophic interactions
in food webs, are often in themselves an important food source in an eco-
system and may modulate the effects of contaminants in hosts (Lafferty
et  al., 2008; Johnson et  al., 2010). Parasites can provide information on
the presence of, and direct or indirect interactions with, sympatric spe-
cies as well as temporal and spatial patterns of habitat use (Hoberg, 2010).
Healthy ecosystems typically have a diverse assemblage of parasites,
reflecting diversity of definitive and intermediate host species and vec-
tors. Detection of the ‘normal’ complement of parasites can be indicative
of a healthy ecosystem (Hudson et al., 2006). Conversely, detection of non-
endemic/invasive parasites or a depauperate parasite community can
suggest otherwise. Contemporary arctic host–parasite assemblages have
been strongly influenced by dynamic shifts in climate and invasive pro-
cesses, particularly over the Pleistocene. Parasites can thus also reflect and
provide insights into host evolutionary history and the complex historical
interactions that have structured ecosystems in space and time (Hoberg
and Brooks, 2008; Hoberg et al., 2012c).
To use parasites as indicators, and to track and predict changes in
parasitism and animal health, comprehensive data on parasite biodiver-
sity, distribution and lifecycles are required (Hoberg et al., 2003; Hoberg
and Brooks, 2008; Hoberg et al., 2008b). Although considerable progress
in defining the diversity and ecology of parasites of arctic ungulates has
been made, there remain substantial knowledge gaps. In this chapter, we
review the current known biodiversity, ecology and impacts of parasites
in arctic ungulates of North America, including Greenland. We identify
knowledge gaps and emerging issues and suggest future research direc-
tions. We define ‘arctic’ ungulates as those species naturally and consis-
tently found in the subarctic and arctic regions as outlined by Conservation
of Arctic Flora and Fauna (CAFF) (Fig. 2.1) and focus on caribou (Rangifer
tarandus ssp.), muskoxen (Ovibos moschatus ssp.), moose (Alces americanus
ssp.) and Dall’s sheep (Ovis dalli dalli).


2.2.1. Caribou – Rangifer tarandus ssp.

Caribou and reindeer are widespread and abundant across the North
American (Figs. 2.2a–c), European and Asian Arctic regions, with a global
population of 3.8 million individuals and an estimated North American
104     Susan J. Kutz et al.

FIGURE 2.1  Map of the North American Arctic showing important political and
­geographic boundaries, including definition of the Subarctic, low and high Arctic. The
latter information adapted from Conservation of Arctic Flora and Fauna (CAFF, 2010).
Map created by N. Pamperin, Alaska Department of Fish and Game.

population of approximately 1.5 million (Geist, 1998; Vors and Boyce,

2009; Russell and Gunn, 2010). Through subsistence harvests, sport hunt-
ing and tourism, caribou are important sources of food and income for
northern aboriginal people as well as a key focus for many traditional
activities (Ferguson and Messier, 1997; Jean and Lamontagne, 2004). Meat
replacement value for a caribou carcass in the North American Arctic is
estimated to be between C$500 and 1,000 and represents a market of tens
of millions of dollars per year (Usher, 1976; Ashley, 2000; Tesar, 2007).
Several subspecies and ecotypes of caribou are recognized in North
America (Banfield, 1961; Miller, 1998); however, the current classification
is likely to be modified by recent genetic studies (McDevitt et  al., 2009;
Courtois et al., 2010; Festa-Bianchet et al., 2011). Here, we include all extant
Rangifer subspecies living in the high, low and subarctic and define them
based both on ecotype and current subspecies designation. This includes
the migratory barren-ground caribou (R. t. groenlandicus) occurring in
several disjunct populations in Greenland and across most of the main-
land tundra in NU and NT, Canada; forest and migratory Grant’s caribou
(R. t. granti) in YT and AK; forest (boreal) and mountain dwelling wood-
land caribou (R. t. caribou) throughout the boreal forest and mountain
regions and migratory woodland caribou in northern Quebec (QC) and
Parasites in Ungulates of Arctic North America and Greenland    
FIGURE 2.2  Distribution of caribou in (A) Canada and Alaska, USA (ecotypes indicated).

106     Susan J. Kutz et al.

FIGURE 2.2—cont’d  (B) Greenland. (C) An adult male Dolphin-Union caribou. Canada/
Alaska map created by N. Pamperin and J. Wells, Alaska Department of Fish and Game.
Greenland map adapted from that by Christine Cuyler, Greenland Institute of Nature.
Caribou photograph by S. Kutz. (For color version of this figure, the reader is referred to
the web version of this book.)
Parasites in Ungulates of Arctic North America and Greenland     107

Labrador; Peary caribou (R. t. pearyi) on the arctic islands and introduced
Eurasian semi-domesticated reindeer (R. t. tarandus) in western AK, near
Tuktoyaktuk, NT, and in various locations in Greenland.
Caribou in North America are thought to have been isolated in two
separate glacial refugia during the terminal Pleistocene. Rangifer t. pearyi,
R. t. groenlandicus and R. t. granti originated from the Beringian–Eurasian
lineage and R. t. caribou originated from the North American lineage
which was isolated south of the ice sheets and then rapidly spread north
and west across the boreal region in the Holocene (Flagstad and Røed,
2003; Cronin et al., 2005; Røed, 2005; McQuade-Smith, 2009). The historical
biogeography of Rangifer species, together with differences in ecology
among ‘ecotypes’, and multiple introductions and subsequent move-
ments of Eurasian reindeer in the late 1800s and early 1900s (Siem, 1913),
no doubt has had an important influence on the contemporary parasite
fauna (Lankester and Fong, 1989; Hoberg et al., 2012c).
Migratory caribou herds naturally undergo substantial cyclic fluctua-
tions with more than a 10-fold change in population size (Bergerud, 2000;
Couturier et al., 2004). Additive anthropogenic stressors and direct mor-
tality, such as hunting and injury loss, as well as industrial development,
roads, climate change and disease, are thought to have significant impacts
and may exacerbate the episodic population fluctuations (Forchhammer
et al., 2002; Kutz et  al., 2009b; Vors and Boyce, 2009; Russell and Gunn,
2010; Festa-Bianchet et al., 2011).
Pronounced population cycles are not recognized for woodland cari-
bou but significant declines in population size and range for this subspe-
cies have been attributed mainly to anthropogenic disturbance and habitat
loss (Vors et al., 2007; Festa-Bianchet et al., 2011; Wasser et al., 2011). For
Peary caribou on the high arctic islands, periodic events of icing of the
snow surface, which prevent access to food, are considered a major cause
of starvation-related mortality (Miller and Barry, 2009). Peary caribou and
woodland caribou are considered ‘endangered’ or ‘threatened’ across most
of their range and barren-ground caribou are listed as ‘of special concern’,
by the Species at Risk Act in Canada (

2.2.2. Muskoxen – Ovibos moschatus ssp.

Muskoxen are the second most abundant ungulate in the Arctic and, as with
caribou, they serve as an important source of subsistence food and income
for aboriginal people, the latter through commercial and sport hunting and
sale of fibre (qiviut) (Nuttal et al., 2010). Unlike caribou, they are relatively
sedentary animals and do not undergo extensive seasonal migrations.
There are two recognized subspecies of muskoxen, both of which have
been influenced by historical extinction and extirpation as well as recent
patterns of introduction. Ovibos moschatus moschatus is endemic on main-
108     Susan J. Kutz et al.

land NT and NU whereas the ‘island’ or ‘white-faced’ muskox, O. m. war-

dii, has ranged historically across most of the arctic islands and eastern
Greenland (Fig. 2.3a–c) (Campos et  al., 2010). There are approximately
105,000 naturally occurring individuals in the NT and NU (Anonymous,
2011b). They are most abundant on Victoria and Banks Islands, Canada,
and have been harvested commercially at these locations since the mid-
1970s to provide meat and fibre for sale to the public (Gunn et al., 1991b).
The population in east Greenland is over 10,000 (C. Cuyler, pers. comm.).
In addition to these naturally occurring populations, a number of trans-
located herds are established in AK, YT, northern QC and west Greenland.
Ovibos m. wardi herds in AK and YT resulted from a series of translocation
events that began in 1930 with 34 muskoxen from east Greenland brought to
Fairbanks, AK, via the Copenhagen Zoo. In 1935–1936, 31 muskoxen from
Fairbanks were introduced to Nunivak Island, AK in the Bering Sea. These
animals thrived and created a source population of animals that have since
been transplanted to various locations around AK (Paul, 2009). Today, there
are approximately 4750 muskoxen in AK (Harper, 2009). Range expansion
of a population introduced to northeast AK has resulted in approximately
150–200 muskoxen in YT and NT west of the Mackenzie River (Gunn et al.,
1991b; Reynolds, 1998; ADFG, 2011b; Anonymous, 2011a,b).
Ovibos m. wardi were also introduced to northern QC in 1967. Fifteen
muskoxen were translocated from Ellesmere Island (NU) and held cap-
tive near Kuujjuaq as an agricultural initiative (Le Hénaff and Crête, 1989).
Between 1973 and 1983, this herd was gradually released from captive
management and the free-ranging population has grown in size to approx-
imately 1500–2000 individuals ranging mainly between the communities
of Kuujjuaq and Tasiujaq, QC and gradually expanding into Labrador
(Chubbs and Brazil, 2007).
Twenty-seven muskox calves from east Greenland were translocated
to the Kangerlussuaq region in west Greenland from 1962–1965 via the
Copenhagen Zoo. This population subsequently served as the source pop-
ulation for several more translocations in west Greenland (Clausen, 1993)
(Fig. 2.3b). These series of translocations and introductions (in Greenland,
Alaska and Canada) has likely influenced the diversity and distribution
of parasites in muskoxen, and perhaps sympatric species, in the Arctic
(Hoberg et al., 1999; Kutz et al., 2007).

2.2.3. Moose – Alces americanus ssp.

Two subspecies of moose are found in the North American Arctic (Fig. 2.4a
and b). East of the Mackenzie Mountains are Alces a. andersoni and in and
to the west of the mountains is the much larger subspecies A. a. gigas (Bow-
yer et al., 1998; Hundertmark and Bowyer, 2004). Approximately 275,000
moose are found in arctic North America with the vast majority of these
Parasites in Ungulates of Arctic North America and Greenland     109
FIGURE 2.3  Distribution of muskoxen in (A) North America.
110     Susan J. Kutz et al.

FIGURE 2.3—cont’d (B) Greenland. Translocations of muskoxen to east Greenland indi-

cated. ©. (C) Adult male muskoxen, O. m. wardi, from Victoria Island, Nunavut. Canada/
Alaska map created by N. Pamperin and J. Wells, Alaska Department of Fish and Game.
Greenland map adapted from that by Christine Cuyler, Greenland Institute of Nature.
Muskox photograph by S. Kutz. (For color version of this figure, the reader is referred to
the web version of this book.)
Parasites in Ungulates of Arctic North America and Greenland     111

FIGURE 2.4  (A) Distribution of moose in arctic and subarctic North America, (B) Alaskan
moose (A. a. gigas). Map created by N. Pamperin and J. Wells, Alaska Department of Fish
and Game. Moose photograph by J. Jemison, Alaska Department of Fish and Game. (For
color version of this figure, the reader is referred to the web version of this book.)

(~200,000) in AK; 65,000 in YT and 10,000 in NT and NU (Franzmann and

Schwartz, 1998). Moose are not present in Greenland. There have been
moose translocations within AK (Paul, 2009) but no introductions of moose
into northern Canada or AK.
Although primarily forest dwelling, both subspecies are found along
rivers and lake shores on the tundra extending north to the arctic coast.
Moose are an extremely important source of food for people in the boreal
forest regions across northern Canada and AK (Lynch, 2006; Larter, 2009).
112     Susan J. Kutz et al.

FIGURE 2.5  (A) Distribution of Dall’s sheep in arctic and subarctic North America,
(B) Adult male Dall’s sheep. Map created by N. Pamperin and J. Wells, Alaska Department
of Fish and Game. Photograph by S. Arthur Alaska Department of Fish and Game. (For
color version of this figure, the reader is referred to the web version of this book.)

2.2.4. Dall’s Sheep – Ovis dalli dalli

Dall’s sheep are common, occurring in disjunct populations throughout
the mountainous regions of AK and the western Canadian Arctic and Sub-
arctic (Fig. 2.5b) (ADFG, 2011a; Anonymous, 2011c; ENR, 2011). There are
approximately 45,000 in NU and NT and 50,000–64,000 in AK. They are
absent from the Arctic islands and Greenland. In general, populations are
healthy and stable across their range. Dall’s sheep have not been translo-
cated within the Canadian North and only a single unsuccessful introduc-
tion has occurred in AK (Paul, 2009). There is some subsistence hunting
of Dall’s sheep as well as a strong recreational-hunting industry that pro-
vides significant income to the northern economy (e.g., ENR, 2011).
Parasites in Ungulates of Arctic North America and Greenland     113

2.2.5. Other ungulate hosts

Mountain goats (Oreamnos americanus) just barely extend into the subarc-
tic in southern AK, and the Mackenzie Mountains, NT and southern YT,
Canada. Population numbers are low and these animals are not used to
any significant extent for food or sport hunting. Mountain goats have a
distributional history in western North America, which parallels that of
wild sheep, with both being represented by strongly disjunct populations
across mountainous terrain (Loehr et al., 2006; Shafer et al., 2011). Com-
pared to other arctic ungulates, these ranges indicate relatively limited
vagility, which may be expected to have an influence on the distribution
of parasites (Hoberg et al., in press-a).
Wood bison (Bison bison athabascae), introduced plains bison (Bison bison
bison), mule deer (Odocoileus hemionus), Sitka black-tailed deer (Odocoileus
hemionus sitkensis), occasionally white-tailed deer (Odocoileus virginianus) and
elk (Cervus elaphus) are found in the Subarctic as defined by CAFF and have
distributions that are either parapatric (with minimal overlap) or have some
degree of sympatry with the arctic ungulate species described above. These
other bovids and cervids are more typical of temperate ecosystems. Although
introduced elk populations are established in southern and central YT, these
will not be considered in detail in this chapter. They are, however, potentially
important in the context of ecological perturbation and northward range
expansion and invasion for assemblages of hosts and parasites (e.g. Hoberg
and Brooks, 2008; Kutz et al., 2009b; deBruyn, 2010; Hoberg, 2010).

Nematodes are important parasites in ungulates globally (Anderson,
2000). Nematodes of the orders Strongylida, Oxyurida, Trichocephalida
and Spirurida are found in ungulates of Arctic North America and more
broadly across the Holarctic region (Priadko, 1976). Species among these
orders are found in a variety of developmental stages in almost all host
tissues and maintain a diversity of lifecycles.

2.3.1. Nematodes of the gastrointestinal tract

Gastrointestinal nematodes of arctic ungulates are referred to three orders,
including Strongylida, Oxyurida and Trichocephalida. The strongyles,
or bursate nematodes, are the most diverse and abundant. Among the
stronglyes, members of the subfamilies Ostertagiinae and Nematodiri-
nae are dominant in terms of taxonomic and numerical diversity (Hoberg
et al., 2001) (Fig. 2.6). Species richness in these groups is the greatest in the
Palaearctic coinciding with a Eurasian centre of origin for the fauna and
declines on a longitudinal gradient from west to east into North America
114     Susan J. Kutz et al.

FIGURE 2.6  Gastrointestinal nematodes reported from ungulates of arctic North

America, including Greenland. Nomenclature is consistent primarily with Anderson
(2000), with some modifications within the Strongylida (Hoberg and Lichtenfels, 1994;
Durette-Desset al., 1994, 1999; Carreno and Hoberg, 1999; Chilton et al., 2006).

(Hoberg et  al., 2012c). Adult nematodes of most species, including both
males and females, generally can be identified on the basis of morphology
(e.g. Lichtenfels and Pilitt, 1983a; Lichtenfels and Hoberg, 1993). In contrast,
diagnostics at the generic and species level for eggs and larvae remains
problematic but is increasingly being addressed through ­application of
DNA-based techniques (reviewed in Lichtenfels et  al., 1997; Dallas et  al.,
2000a,b). Integrated methods incorporating both morphological characters
for adults and molecular sequence data for adults and larvae are now con-
sidered standard in conducting survey and inventory and for exploring the
occurrence of cryptic diversity in ungulate nematode faunas (e.g. Hoberg
et al., 2001; Leignel et al., 2002; Jenkins et al., 2005a).
(a) Host and Geographic Range. Knowledge of the diversity and host and
geographic distributions of gastrointestinal nematodes in ungulates of
arctic North America and Greenland is based primarily on cross-sectional
and opportunistic studies focussed on a single host species or at a single
location (e.g. Gibbs and Tener, 1958; Nielsen and Neiland, 1974; Samuel
and Gray, 1974; Fruetel and Lankester, 1989; Korsholm and Olesen, 1993;
Simmons et al., 2001). Ostertagiines (species of Teladorsagia, Ostertagia and
Marshallagia) and Nematodirines (species of Nematodirus and Nematodire-
lla) are found in mixed species infections in individual hosts across most of
their range whereas the occurrence of Oxyuridae and Trichuridae is more
variable among regions and host species. Many of these parasites can infect
Parasites in Ungulates of Arctic North America and Greenland     115

a variety of ungulate species but their relative abundance differs across

hosts and geographic regions. For abomasal nematodes, Ostertagia grueh-
neri is most common in caribou; Teladorsagia boreoarcticus is most common
in muskoxen and Marshallagia cf. marshalli is most common in Dall’s sheep
(Nielsen and Neiland, 1974; Fruetel and Lankester, 1989; Hoberg et al., 1999;
Simmons et al., 2001). In caribou and muskoxen, Marshallagia tends to be
restricted to the mountainous regions and arctic islands and is uncommon
on the mainland tundra. For the Nematodirinae, species diversity and abun-
dance tend to be greater in muskoxen and Dall’s sheep compared to caribou
and moose (Nielsen and Neiland, 1974; Hoberg et al., 2001). One exception
may be the Kangerlussuaq-Sisimiut caribou herd of west Greenland where
faecal examinations revealed an unusually high prevalence of ­nematodirine
eggs in adult females (J. Steele, S. Kutz, C. Cuyler, unpubl. data).
(b) Ecology. The ostertagiine and nematodirine nematodes infecting
northern ungulates have direct life cycles. Adults live in the gastrointesti-
nal tract and eggs are shed in the host’s faeces. Larval development to the
infective third stage (L3) occurs in the external environment and develop-
ment and survival rates are related to climatic condition (O’Connor et al.,
2006). Development of larvae to the infective stage may occur before
(Nematodirinae) or after (Ostertagiinae) hatching from the egg. For the
Trichuridae, the infective larva remains in the egg. Infective larvae (or
eggs with L3) are passively ingested by the final hosts during grazing.
Eggs and/or larvae of some species in domestic ungulates can persist in
the environment over winter if not ingested by a host within the first year
(O’Connor et al., 2006). Once ingested, larvae pass through the digestive
tract until they reach their final location in either the abomasum or the
intestine. Here, the larvae migrate into the mucosa where they develop to
a fourth larval stage (L4). Development to adults is typically completed
in the lumen. Under certain environmental and/or host conditions, the
L4 of several ostertagiine nematodes may undergo inhibited develop-
ment in the mucosa, delaying the completion of their life cycle for several
months (Eysker, 1993; Sommerville and Davey, 2002).
(b) Impacts. The impacts of gastrointestinal nematodes on wildlife
species are relatively unstudied, but they can negatively influence body
condition, physiology (notably reproductive success) and behaviour of
free-ranging ungulates (Albon et al., 2002; Stien et al., 2002; Morgan et al.,
2005). In domestic livestock, ostertagiine and nematodirine nematodes
are significant pathogens and can cause subtle to severe disease with
impacts on food intake, nutrient absorption and body condition, ulti-
mately reducing overall productivity (Holmes, 1987). Some of the most
severe disease impacts result from parasites migrating from the mucosa
to the lumen of the gastrointestinal tract during development and tran-
sition from parasitic larvae to adult stages (Myers and Taylor, 1989).
The Trichuridae tend to be parasites of young animals and can cause
116     Susan J. Kutz et al.

significant diarrhoea in heavily infected domestic livestock. The Oxy-

uridae do not appear to cause significant production loss in domestic
livestock. Subfamily Ostertagiinae

Nomenclature and Taxonomy

Trichostrongyline nematodes of the subfamily Ostertagiinae are
­common abomasal parasites of arctic ungulates. Challenges associated
with defining species limits within this group have hindered the under-
standing of the geographic patterns and host associations of these par-
asites (Dróżdż, 1995). In parallel to most helminth groups, numerous
generic and species designations have been assigned over time and eval-
uation of the literature requires a knowledge of these synonymies. This
problem is heightened among the ostertagiines because polymorphism
(multiple morphologically distinct forms within a species) occurs among
adult males in five of 15 genera of the subfamily (Dróżdż, 1995; Hoberg
et  al., 2009). For example, historically for some species, discrete differ-
ences in structural characters of the genital cone and spicules resulted in
identification of individuals as different nominal species, often in separate
genera (Gibbons and Khalil, 1982). Only later was it recognized that these
morphological differences defined the major and minor morphotypes of
single species (Dróżdż, 1995). Since the recognition of polymorphism in
the 1970s, the phenomenon has been extensively corroborated based on
cross-breeding experiments, morphology, ecological studies and DNA
sequence data (Daskolov, 1974; Dróżdż, 1974; Lancaster and Hong, 1981;
Lichtenfels and Hoberg, 1993; Dróżdż, 1995; Hoberg et  al., 1999, 2001).
Major morphotypes are defined by their numerical dominance (relative to
minor morphotypes) within infrapopulations of single hosts and appear
to represent a balanced polymorphism (Daskolov, 1974; Dróżdż, 1974;
Dróżdż, 1995), although seasonal variation in relative abundance has been
noted (e.g. Hoberg et al., 1999). The recognition, application and misap-
plication of polymorphism among males have considerably confused the
taxonomy and description of ostertagiinae genera and species over the
past century (Dróżdż, 1995; Hoberg et  al., 1999). Several arctic osterta-
giines, including species of Ostertagia, Teladorsagia and Marshallagia, are
polymorphic (Table 2.1) (Lichtenfels and Pilitt, 1989; Lichtenfels et al., 1990;
Hoberg et al., 1999; Hoberg et al., in press-a,b). Throughout the chapter,
we adopt the following convention for naming these polymorphic species.
When it first appears in the text, the latin binomials are presented for each
morphotype, with the major morph given first, for example, Marshallagia
marshalli/M. occidentalis, Teladorsagia circumcincta/T. trifurcata/T. davtiani
or T. boreoarcticus f. major/f. minor A/f. minor B in the standard notation
Parasites in Ungulates of Arctic North America and Greenland     117

TABLE 2.1  Major and minor morphs for ostertagiines recovered from arctic host species

Major morphotype Minor morphotype

Marshallagia marshalli M. occidentalis

Marshallagia lichtenfelsi f. minor
Ostertagia gruehneri O. arctica
Teladorsagia boreoarcticus f. minor A, f. minor B
T. circumcinctaa T. trifurcata/T. davtiani
a Is
included here for completeness; however, most, if not all records likely represent T. boreoarcticus or
an as yet unidentified species (Hoberg et al., 1999, 2001, 2012a, 2012b).

currently adopted (Dróżdż, 1995; Hoberg et al., 1999). Following this first
appearance in the text, we dispense with the exhaustive listing and use
only the nominal major ­morphotype to designate the species.
Another more general issue that affects our understanding of diversity
for trichostrongyloids is the presence of cryptic species (Pérez-Ponce de
Leon and Nadler, 2010). An example is T. boreoarcticus described from mus-
koxen of the central Canadian Arctic in 1999 (Hoberg et al., 1999). Prior to
the description of this species, all arctic specimens of Teladorsagia were iden-
tified as T. circumcincta or one of its minor morphotypes, which are common
parasites of domestic sheep (Hoberg et al., 2012b). Teladorsagia circumcincta
was considered to represent a morphologically variable taxon with a con-
siderable host range and broad geographic distribution and as such was
an example of a widespread species (Hoberg et al., 1999). This species and
T. boreoarcticus are similar in appearance but can be distinguished on the
basis of morphological characteristics and mitochondrial DNA and it is now
known that Teladorsagia sp. in muskoxen across their North American range
is T. boreoarcticus (Hoberg et al., 1999). The discovery of T. boreoarcticus may
indicate the occurrence of a taxonomically diverse complex of cryptic spe-
cies within Teladorsagia circulating in domesticated and free-ranging ungu-
lates. The species limits for this complex have yet to be adequately explored
(Hoberg et  al., 1999; Leignel et  al., 2002; Hoberg et  al., 2012b) but have
fundamentally changed our understanding of the history, structure and
diversity of ungulate helminth faunas in the Holarctic region (e.g. Hoberg
et al., 2008a; Hoberg, 2010). Another cryptic species within the Teladorsagia
complex has also been proposed at temperate latitudes (Leignel et al., 2002;
Grillo et al., 2007) and species complexes may also exist for Marshallagia in
North American ungulates (Lichtenfels et al., 1997; Hoberg et al., 2012a). Ostertagia gruehneri/O. arctica

(a) Host and Geographic Distributions. Across the Holarctic region, O. grueh-
neri is the most common gastrointestinal nematode of all subspecies of
­Rangifer with prevalence approaching (Table 2.2) 100% both within and
118     Susan J. Kutz et al.

TABLE 2.2  Gastrointestinal nematodes reported from ungulates of arctic North

America, including Greenland. The range of prevalence reported is indicated below the
parasite name. Only prevalence estimates based on sufficient sample sizes are included.
Data compiled from available published and grey literature.

Host, Parasite
(range of prevalence) Herd, region or nearest place name

Marshallagia marshalli AK Not specifieda; Fairbanksb
NT Banks Islanda,b
NU Dolphin-Unionc; Kugluktuka
GL Kangerlussuaq-Sisimiutd
Ostertagia gruehneri AK Not specifiede; Spruce Creek, Mulchatna,
Northern Alaska Peninsulab
YT Chisanaf
NT Beverlye,g;Bathursth
NU Kugluktuka; Dolphin-Unionc;
Not specifiede; Bathurst Islandb
GL Akia-Maniitsoqi
Teladorsagia boreoarcticus AK Golovinj; Unalakleet j; Mulchatna,
Northern Alaska Peninsulab
YT Chisanaf
NT Banks Islandk; Hope Lakej; Bathursth
NU Dolphin-Union k; Kugluktukb
Teladorsagia circumcinctaw AK Not specifiedl
NT Beverlyg
NU Dolphin-Unionc
GL Kangerlussuaq-Sisimiute
Nematodirella AK Not specifiedm; Egavik, Kivalina,
longissimespiculata Fakotna, Round Upb
NT Beverlyg
Nematodirus tarandi AK Takotnab
NT Beverlyg
Skrjabinema tarandi AK Arctic Slope; Barrow; Brooks Rangen
NT Beverlyg,n
Dall’s sheep
Cooperia spp. AK Granite Mountainso
Marshallagia marshalli - AK Dry Creek, Kenai Peninsula, Interioro;
(18–100%) Not specifiedu
NT Central Mackenzie Mountainsp
Ostertagia gruehneri NT Central Mackenzie Mountainsp
Ostertagia gruehneriy (8%) AK Dry Creek, Interioro
Parasites in Ungulates of Arctic North America and Greenland     119

TABLE 2.2  (continued)

Host, Parasite
(range of prevalence) Herd, region or nearest place name
Teladorsagia circumcincta ## AK Dry Creek, Interior, Kenai Peninsulao
Nematodirella species AK Dry Creeko
Nematodirus archari or AK Dry Creeko,q; Kenai Peninsulao
N. andersoniy (58–82%) NT Central Mackenzie Mountainsp
Nematodirus davtiani AK Dry Creek, Kenai Peninsulao
(48–77%) NT Central Mackenzie Mountainsp
Nematodirus oiratianus AK Dry Creek, Kenai Peninsulao;
(13–65%) Not specifiedv
NT Central Mackenzie Mountainso
Nematodirus spathiger AK Dry Creek, Kenai Peninsulao
(38–83%) NT Central Mackenzie Mountainsp
Skrjabinema sp. (19,100%) AK Windy Gap, South Central; Dry Creek,
Kenai Peninsulao
Skrjabinema ovis NT Central Mackenzie Mountainsp
Trichuris sp. (25–85%) AK Windy Gap, South Central; Dry
Creek, Granite Mountains, Kenai Pen-
Trichuris schumakovitschi NT Central Mackenzie Mountainsp
Nematodirella alcidis AK Not specifieda,m; Palmerb
Marshallagia marshalli AK Not specifieda,m,u
NT Banks Islandb
NU Devon and Ellesmere Islandsr; Victoria
Marshallagia species AK Nunivaks
NU Bathurst Islands
Teladorsagia boreoarcticus AK Barter Islandj
(100%) NT Banks Islandb,h
NU Cox Lake and Rae River near Kugluk-
tuk; Victoria Island (Ekalluk River) j;
Ellesmere Islandj,r
Teladorsagia circumcincta ## NU Thelont; Victoria Islandd
Nematodirella sp. NU Cox Lake near Kugluktukc; Ekalluk
River, Victoria Islandb
Nematodirella alcidis AK Nunavik Islandb
NU Kugluktuka; Victoria Islanda
120     Susan J. Kutz et al.

TABLE 2.2  (continued)

Host, Parasite
(range of prevalence) Herd, region or nearest place name
Nematodirella gazelli NU Bathurst Islandm,s
Nematodirella longissimespiculata AK Barter Islanda; Collegem
NT Banks Islandb
NU Thelon Game Sanctuaryt
Nematodirus helvetianus AK Collegeb
NT Banks, Islandb
NU Banks Devon and Ellesmere Islandsb,r
Nematodirus tarandi AK Nunavik Islandb; Collegeb
NT Aklavikb
NU Rae River and Cox Lakeb; Ekalluk Riverb
a  Hoberg et al. (2001).
b  USNPC, (2011).
c  Hughes et al. (2009);

d  Korsholm and Olesen (1993).

e  Lichtenfels et al. (1990).

f  Hoar et al. (2009).

g  Fruetel and Lankester (1989).

h  B. Hoar, J. Invik, S. Kutz, E. Hoberg (unpubl. obs.).

i  J. Steele, S. Kutz, C. Cuyler, E. Hoberg (unpubl obs.).

j  Hoberg et al. (1999).

k  Hoberg et al., (2012b).

l  Becklund (1962).

m  Lichtenfels and Pilitt (1983a).

n  Schad (1959).

o  Nielsen and Neiland (1974).

p  Simmons et al., (2001).

q  Rickard and Lichtenfels (1989).

r  Webster and Rowell (1980).

s  Samuel and Gray (1974).

t  Gibbs and Tener (1958).

u  Lichtenfels and Pilitt (1989).

v  Lichtenfels and Pilitt (1983b).

w Teladorsagia circumcincta is an apparent misidentification in the Dolphin-Union Herd and should be

referred to T. boreoarcticus (Hoberg et al., in pressb). Other populations of T. circumcincta reported in

northern ungulates (with the possible exception of Greenland) are considered to be T. boreoarcticus
or may be included in a putative complex of species circulating in free-ranging ungulates, which
excludes T. circumcincta (Hoberg et al., 1999, 2001, 2012b).
x Records attributed to Nematodirus archari in Dall’s sheep may be referred to another species endemic

to North America, N. andersoni according to Durette-Desset and Samuel (1989). Additional studies
are required to establish if N. archari is a Holarctic species (Rickard and Lichtenfels, 1989).
y Nielsen and Neiland (1974) originally reported O. ostertagi in Dall’s sheep from Dry Creek, AK.

These specimens were re-determined as O. gruehneri by E.P. Hoberg and A. Abrams. All northern
records of O. ostertagi in isolated populations of free-ranging hosts are likely referable to O. grueh-
Parasites in Ungulates of Arctic North America and Greenland     121

across most caribou and reindeer herds examined (Bye and Halvorsen,
1983; Bye, 1987; Bye et  al., 1987; Irvine, 2000; Irvine et  al., 2001; Hrabok
et al., 2007; Hoar et al., 2009). The ubiquitous nature of O. gruehneri in Rangi-
fer may reflect the biogeographic history for these cervids and ­particularly
the history of expansion for host populations linking Eurasia and North
America, as well as expansion in the Nearctic (Hoberg et al., 2012b).
Ostertagia gruehneri does appear to be absent from one natural popu-
lation of caribou in Greenland. In a small survey of the Kangerlussuaq-
Sisimiut caribou herd in west Greenland, O. gruehneri was not found and
other ostertagiines, Teladorsagia sp. (reported as T. circumcincta but may be T.
boreoarcticus or both) and Marshallagia sp. appeared to dominate the aboma-
sal fauna (Korsholm and Olesen, 1993). Recent post-mortem data support
this pattern and also demonstrate that O. gruehneri is present in the Akia-
Maniitsoq caribou herd immediately to the south of, but physically isolated
from, the Kangerlussuaq-Sisimiut herd (J. Steele, S. Kutz, C. Cuyler unpub.
obs.). Environmental conditions in the Kangerlussuaq region are relatively
mild and generally seem to be suitable for development of O. gruehneri. The
absence of the parasite in this herd may be because it did not establish with
the founding animals or because transmission was not sustained during
periods of low host density. The west Greenland caribou herds were estab-
lished by sporadic natural colonization events by only a few animals, and
these populations have undergone periodic crashes (Meldgaard, 1986; Jep-
sen et al., 2002; Cuyler, 2007). Ostertagia gruehneri is also absent in introduced
reindeer in Iceland where the contemporary parasite fauna consists almost
exclusively of species ­originating from domestic livestock (Gudmundsdottir,
Ostertagia gruehneri occurs in muskoxen but at a much lower prevalence
and intensity than in caribou or reindeer (S. Kutz, E. Hoberg, unpubl. obs.).
In Dall’s sheep, O. gruehneri is uncommon, with sporadic, low-intensity
infections reported primarily in the summer (Nielsen and Neiland, 1974;
Simmons et al., 2001). Unusually high counts of ‘strongyle-type’ eggs were
observed in summer faecal surveys of one population of Dall’s sheep from
the Richardson Mountains, NT (Table 2.3). These eggs were not identified
to species but most likely are either O. gruehneri or T. boreoarcticus. There
is substantial sympatry with large numbers of caribou from the Porcupine
herd as well as with a small population of muskoxen. Spill-over of O. grueh-
neri from caribou, or T. boreoarcticus from muskoxen, is possible. Notably,
a high abundance of strongyle-type eggs has not been reported from other
Dall’s sheep populations sympatric with woodland caribou (Table 2.3).
(b) Ecology. Egg production for O. gruehneri in Rangifer is highly sea-
sonal with faecal egg counts in captive and wild reindeer and caribou
increasing in the spring, remaining high throughout the summer and then
tapering to very low or negative egg counts from late fall through to the
spring (Irvine, 2000; Irvine et  al., 2000; Hoar et  al., 2009,2012a). On the
122     Susan J. Kutz et al.

TABLE 2.3  Prevalence (%) and intensity of eggs (epg) or oocysts/gram (opg) faeces of parasites
detected in faecal samples from North American arctic ungulates from July 2000 to July 2010a

Number of fecals collected each

season Marshallagia sp.

Herd or location State N totalb Winter Spring Summer Fall % Range epg

Banks Island NT 341 122 78 141 57.5 1–65
Sahtu NT 109 73 35 1 0 NA
Chisana Herd YT 158 158 5.4 1–83
Beverly/Qamanirjuaq NT 25 25 0 NA
Bluenose East NT 51 20 0 NA
Bluenose West NT 10 10 0 NA
Cape Bathurst NT 37 37 2.7 77
Dall’s Sheep
Mackenzie Mountains NT 482 66 194 68 154 86.1 1–117
Richardson Mountains NT 262 2 177 60.3 1–111
Sheep Mountain YT 9 9 89.0 1–38
Ivaavik YT 6 6 83.0 2–43
Tombstone Park YT 1 1 0 NA
Various places AK 26 6 4 9 0 NA
Mackenzie Mountains NT 4 4 0 NA
Sahtu NT 36 27 9 11.1 1–27
Central YK 27 17 10 29.6 2–16
Yukon YK 24 0 NA
Ellesmere Island NU 4 4 25.0 4–4
Thelon NU 2 0 NA
Victoria Island NU 28 28 42.9 1–2
Banks Island NT 262 72 10.3 1–13
Sahtu NT 8 8 50 1–3
North YT 19 10 9 0 NA
a Samples were frozen at −20°C and analyzed by modified Wisconsin double-centrifugation sugar
flotation technique (specific gravity 1.26) at the University of Saskatchewan (January 2000–August 2005) and
University of Calgary (September 2005–December 2010). Samples collected as part of a wildlife parasitology col-
laborative monitoring program with the wildlife departments of the governments of the Northwest Territories,
Nunavut and Yukon, US Department of Agriculture, and Universities of Calgary and Saskatchewan.
b In some cases, season of faecal collection was not specified and ‘N’ total is greater than the sum of seasonal ‘N’.

c Includes genera of Trichostrongylinae that produce typical ‘strongyle’ egg. Most likely represents a mixture

of Ostertagia gruehneri and Teladorsagia boreoarcticus, the former most common in caribou and the latter most
common in muskoxen.
Parasites in Ungulates of Arctic North America and Greenland     123

Strongyle eggsc Nematodirinae Trichuris sp. Skrjabinema sp. eggs Eimeria spp.

Range Range Range Range Range Range

% epg % epg % epg % epg % epg % opg

23.8 1–19 15.5 1–46 0 NA 0 NA 39.3 1–170 16.4 1–2000

31.2 1–46 6.4 1–7 0.9 1–1 0.9 1–1 0.9 25 8.3 2–1000
60.8 1–247 0 NA 0 NA 9.5 1–7 12.2 2–63 4.7 1–236
8.0 1–1 0 NA 0 NA 0 NA 0 NA 8.0 8–28

5.9 1–4 0 NA 0 NA 0 NA 7.8 17–677 5.9 2–11

0 NA 0 NA 0 NA 0 NA 0 NA 0 NA
0 NA 5.4 4–77 0 NA 0 NA 8.1 39–139 0 NA

1.9 1–23 78.4 1–205 55.6 1–602 2.3 1–105 11.2 1–634 89.4 1–5000
53.8 1–321 62.6 1–207 40.1 1–97 3.8 1–161 24.4 1–3000 70.2 1–6000
0 NA 89.0 1–7 78.0 1–22 0 NA 0 NA 100 5–1000
83.0 1–15 83.0 5–26 67.0 8–40 0 NA 0 NA 50 558–1500
100 3–3 100 11–11 0 NA 0 NA 0 NA 100 13–13

0 NA 0 NA 0 NA 0 NA 0 NA 0 NA
0 NA 0 NA 0 NA 0 NA 0 NA 0 NA
0 NA 25.0 1–39 0 NA 0 NA 2.8 76–76 0 NA
0 NA 18.5 1–4 0 NA 0 NA 3.8 14–14 0 NA
0 NA 79.2 1–41 0 NA 0 NA 16.7 6–247 0 NA

100 24–59 100 1–16 0 NA 0 NA 50 1–6 100 153–704

50 1–1 0 NA 0 NA 0 NA 50 26 0 NA
0 NA 28.6 1–8 0 NA 0 NA 0 NA 96.4 1–325
76.3 1–2236 62.2 1–603 0 NA 0 NA 25.6 1–3745 59.5 1–17,500
87.5 14–66 37.5 1–3 0 NA 0 NA 0 NA 25.0 500–750
57.9 1–187 68.4 1–14 5.3 1–1 0 NA 10.5 7–18 47.4 1–40
124     Susan J. Kutz et al.

Canadian mainland tundra, eggs deposited from early June through to

early August can develop to L3 within 3–4 weeks, but exceptionally high
mid-summer temperatures (>30°C) may delay development (Hoar et al.,
2012b). Although eggs do not survive freezing (deBruyn, 2010), there is
high overwinter survival of both L2 and L3 on the tundra (Van der Wal
et al., 2000; Hoar et al., 2012b).
Inhibition seems to be a key characteristic of the life history of O. grueh-
neri in barren-ground caribou. Extremely high rates of inhibition were
observed in wild barren-ground caribou and in reindeer experimentally
infected with L3 cultured from a barren-ground caribou source (Hoar et al.,
2012a). Inhibition may be an important strategy of O. gruehneri in barren-
ground caribou, enhancing survival and transmission of the parasite in a
harsh arctic environment where the primary host is migratory. Propensity
for inhibition appears to differ across different ecotypes or subspecies of
caribou and reindeer (Leader-Williams, 1980; Bye and Halvorsen, 1983;
Irvine et al., 2000; Hrabok et al., 2006a; Hrabok et al., 2007) and may be
a more common feature linked to migratory behaviour of caribou and
highly seasonal environments (Hoar et  al., 2012a). Relatively long pre-
patent periods (PPP) for this family of parasites were observed in three
muskoxen infected with O. gruehneri L3 from woodland caribou (two
muskoxen infected with 2500 L3 each on June 7, monitored daily; PPPs 87
and 93 days) and barren-ground caribou (one muskox infected with 7000
L3 in January, monitored weekly; PPP 61 days) (S. Kutz, B. Hoar, L. Polley,
B. Wagner, unpubl. obs.). It is unknown if this reflects a normal maturation
rate (no inhibition) for this parasite in muskoxen or if the ­larvae under-
went a short period of inhibition first.
(c) Impacts. In reindeer, high intensities of infection with O. gruehneri
(>5000 adult nematodes/host) can lead to decreased food intake, weight
loss and reduced pregnancy rates (Arneberg et  al., 1996; Arneberg and
Folstad, 1999; Stien et al., 2002).
Using mathematical models, Albon et  al. (2002) demonstrated the
potential role of O. gruehneri in stabilizing population cycles in Svalbard
reindeer. Svalbard is an excellent study site to investigate the impact of
O. gruehneri on its host population because the parasite assemblage of the
reindeer is simple, dominated by O. gruehneri and M. marshalli and the rein-
deer have no competitors or predators on the archipelago. It is likely that
O. gruehneri plays a role in the population dynamics of other reindeer and
caribou populations but establishing such a link is difficult because of con-
founding factors, including predation, competition, hunting, ­development
and resource exploration and extraction. Teladorsagia boreoarcticus

(a) Host and geographic distributions. Teladorsagia boreoarcticus was origi-
nally described as a dimorphic ostertagiine infecting muskoxen and cari-
Parasites in Ungulates of Arctic North America and Greenland     125

bou from the central Canadian Arctic and low Arctic islands primarily in
the region adjacent to Kugluktuk, NU (Hoberg et al., 1999). Subsequently,
a second minor morphotype designated as T. boreoarcticus minor B was
described based on specimens from Victoria Island and Banks Island, NU
and NT, although this form has yet to be demonstrated in mainland pop-
ulations (Hoberg et al., 2012b). The morphological similarity of T. boreo-
arcticus to T. circumcincta, a cosmopolitan nematode of domestic sheep,
and the possibility of a cryptic species complex of Teladorsagia partitioned
among free-ranging northern ungulates complicates a clear understand-
ing of diversity and host associations (Hoberg et al., 1999; Hoberg et al.,
2012b). Prior to the description of T. boreoarcticus, Teladorsagia specimens
isolated from caribou, muskoxen and Dall’s sheep in the North American
Arctic and from mountain goats in western Canada and the US were iden-
tified as T. circumcincta. It is now known that those from muskoxen and
caribou across Canada are T. boreoarcticus (Hoberg et al., 1999). A recent
study of gastrointestinal parasites of caribou and muskoxen in the cen-
tral Canadian Arctic reports T. circumcincta, not T. boreoarcticus, from both
host species (Hughes et  al., 2009) but this is considered a misidentifica-
tion (Hoberg et  al., 2012b). Unresolved is the identity of Teladorsagia sp.
reported from a small number of muskoxen in an introduced population
near Kangerlussuaq, west Greenland. These animals originated from a
natural population in east Greenland and spent time in the Copenhagen
Zoo before arriving at their final destination (Clausen, 1993). Korsholm
and Olesen (1993) reported T. circumcincta in these muskoxen. Although T.
boreoarcticus would be expected in the source population, it is possible that
the animals may have become infected with T. circumcincta in the Copen-
hagen Zoo and maintained that parasite following introduction. Sympat-
ric caribou of the Kangerlussuaq-Sisimiut herd are also host to Teladorsagia
cf. boreoarcticus (J. Steele, S. Kutz, E. Hoberg, C. Cuyler unpubl. data).
The possibility of multi-species infections of Teladorsagia in Greenland is
consistent with the development of mosaic faunas that may be mixtures
of endemic and introduced species (Hoberg et  al., 2012a; Hoberg, 2010;
Hoberg et al., 2012c).
Teladorsagia boreoarcticus is by far the dominant abomasal nematode
of free-ranging muskoxen and is also reported in woodland and bar-
ren-ground caribou and reindeer (Hoberg et al., 1999; Hoar et al., 2009;
deBruyn, 2010). Prevalence and intensity in caribou is generally low, but
woodland caribou can maintain T. boreoarcticus in the absence of musk-
oxen (Hoar et al., 2009; deBruyn, 2010). Adults of T. cf. boreoarcticus, but
not O. gruehneri, were found in two of the now extirpated caribou in Banff
National Park, AB (latitude 51° 8’ 60 N) (deBruyn, 2010), demonstrat-
ing a broad latitudinal distribution for T. boreoarcticus. Teladorsagia sp. is
uncommon in Dall’s sheep and the few reports of T. circumcincta (and
morphotypes) in this host, and the more common reports in mountain
126     Susan J. Kutz et al.

goats (Cowan, 1951; Kerr and Holmes, 1966; Nielsen and Neiland, 1974;
Samuel et al., 1977), may be T. boreoarcticus or involve undescribed species
in a broad complex that remains to be fully characterized (Hoberg et al.,
The complexity associated with defining species limits and diver-
sity within Teladorsagia (and the identification of T. boreoarcticus) clearly
indicates the potential outcomes of incorrect identifications: (i) errone-
ous interpretations about evolutionary history and host associations (e.g.
Brooks and Hoberg, 2006) and (ii) assumptions about life-history char-
acteristics that may not be applicable to the parasite species in question.
Although the extent of this assemblage in free-ranging hosts across the
Holarctic remains unresolved, current evidence suggests that T. circum-
cincta sensu stricto, T. boreoarcticus and a putative array of cryptic species
have been on divergent evolutionary trajectories for a considerable period
of time (Hoberg et al., 1999; Leignel et al., 2002). This has implications for
parasite development and behaviour in an array of free-ranging ungulate
hosts at high latitudes.
(b) Ecology. Preliminary investigations on the ecology of T. ­boreoarcticus
have revealed some key features of this parasite’s life cycle. Based on
faecal surveys of free-ranging populations in northern Canada, there is
a seasonal pattern of egg production with high egg counts throughout
the summer and very low egg production during the winter (S. Kutz,
B. Wagner, L. Polley unpubl. obs.; Samuel and Gray, 1974), a similar pat-
tern to that of O. gruehneri. Eggs can hatch after short periods of freezing
(1–2 weeks at zero to −20°C) (S. Kutz, B. Wagner, L. Polley unpubl. obs.)
but freeze tolerance of larval stages has not been investigated. In prelimi-
nary laboratory studies, eggs developed to L3 within 8–11 days on the
laboratory countertop (estimate 20–22°C) (S. Kutz, B. Wagner, L. Polley
unpubl. obs.).
The life cycle of T. boreoarcticus has been completed experimentally
in three captive muskoxen (S. Kutz, B. Wagner, L. Polley unpubl. obs.).
Eggs originated from free-ranging muskoxen on Banks Island. One
male castrate muskox was experimentally infected with L3 cultured
from eggs that had been frozen for 1–2 weeks. Approximately 950 L3
were given by stomach tube on 21 June and the muskox did not shed
eggs until the following spring, on 11 March. Two female muskoxen
were each experimentally infected with 23,000 L3 of T. boreoarcticus
on 7 September of the same year and did not shed eggs until 24 May.
These results suggest a strong tendency towards larval inhibition and
are particularly surprising for the muskox infected in June when nor-
mal maturation of the parasite would have been expected. One domes-
tic sheep infected with 23,000 L3 on 7 September shed small numbers
of strongyle eggs intermittently from 5 October to 1 March, when egg
production increased significantly for a few weeks and then dropped
Parasites in Ungulates of Arctic North America and Greenland     127

abruptly (S. Kutz, J. Heath, B. Wagner, L. Polley unpubl. obs.). Data

from free-ranging muskoxen indicate that larval inhibition occurs in the
wild. Emergence of larvae from the abomasal mucosa occurs in May
and causes significant pathology including inflammation and oedema
(Kutz et al., 2004b).
(c) Impacts. Teladorsagia boreoarcticus may play an important ecological
role in the population health of muskoxen. High intensities of infection
and abomasitis occur in muskoxen on arctic islands in Canada (Tessaro
et al., 1984; Wobeser, 1984; Blake, 1985; Rowell, 1987; Kutz et al., 2004a) and
it has been suggested that infections in muskoxen may contribute to pop-
ulation cycling through impacts on host body condition and ­reproduction
(Kutz et al., 2004a). Marshallagia marshalli/M. occidentalis

(a) Host and Geographic Distributions. Species of Marshallagia are poly-
morphic abomasal parasites of ungulates across the Holarctic region
(Boev et  al., 1963; Hoberg et  al., 2001). The species in muskoxen, cari-
bou and Dall’s sheep across their range has been identified as M. mar-
shalli, a presumptive Holarctic species, but may represent a component
of a broader cryptic complex (Lichtenfels and Pilitt, 1989; Hoberg et al.,
2012a). In caribou and muskoxen from Canada and Greenland, M. mar-
shalli appears to be more common in relatively xeric areas, including
alpine regions and on the high arctic islands, compared to the low-lying
mainland (Table 2.2). Marshallagia marshalli is present in the Kanger-
lussuaq caribou and muskox herds of west Greenland but absent from
the Akia–Maniitsoq caribou immediately to the south (Korsholm and
Olesen, 1993; Steele et al., 2012). Marshallagia marshalli is the dominant
abomasal nematode in Dall’s sheep across their range. A previously
unknown species of Marshallagia was recently identified in mountain
goats from the western cordillera of North America and appears to be
specific to this host species and common across its range (Hoberg et al.,
2012a.). The northern extent of the range for this species remains unde-
fined, although it is likely to be in sympatry with populations of M.
marshalli in areas where Dall’s sheep and mountain goats are in contact
(Hoberg et al., 2012a).
(b) Ecology. Marshallagia marshalli has a direct life cycle with second-
stage larvae hatching from eggs and developing to L3 in the environment
(Anderson, 2000). Freeze-tolerant eggs make it well suited for the Arctic.
In a preliminary study, Marshallagia eggs collected from Dall’s sheep in the
Richardson Mountains, NT, remained viable after being frozen at −10 to
−20°C for at least 8 months (S. Kutz, J. Heath, B. Wagner, L. Polley unpubl.
obs.). These eggs were isolated and cultured according to Hubert and Ker-
boeuf, (1984) and L3 were recovered after 13–14 days on the laboratory
countertop (estimate 20–22°C). A captive Dall’s × Stone (Ovis dalli stonei)
128     Susan J. Kutz et al.

sheep hybrid infected with 2700 L3 cultured from these eggs became
patent at 29 days post-infection (S. Kutz, J. Heath, B. Wagner, L. Polley
unpubl. obs.).
Egg production of Marshallagia has a seasonal pattern that is the reverse
of that for O. gruehneri and T. boreoarcticus; for muskoxen and Svalbard
reindeer, it is higher in the winter/spring than in the summer months
(Samuel and Gray, 1974; Irvine et al., 2000) (Table 2.3). Winter transmis-
sion is reported for reindeer (Halvorsen et al., 1999; Irvine et al., 2001) and
saiga antelope (Morgan et al., 2006) and is probable for muskoxen, caribou
and Dall’s sheep.
(c) Impacts. Marshallagia spp. are common, and sometimes numeri-
cally dominant, members of the gastrointestinal parasite fauna of arctic
ungulates. Despite this, very little is known about the life history or
host impacts of this genus. In studies in AK and the Mackenzie Moun-
tains, NT, in the 1970s, adult parasite counts in Dall’s sheep ranged to
>2000 but most animals tended to have <1000 adult worms (Nielsen
and Neiland, 1974; Simmons et  al., 2001). The infection intensity of
adult Marshallagia in Dall’s sheep ewes of the Mackenzie Mountains,
NT, was negatively correlated with both host body condition and
pregnancy rates (S. Kutz, N. Simmons, A. Veitch, L. Polley, E. Hoberg
unpubl. obs.). The impacts of M. marshalli in muskoxen and caribou
remain unknown. Subfamily Nematodirinae

Nematodirines are nematodes of the small intestines of ruminants and
lagomorphs (Hoberg, 2005). The subfamily includes species of two gen-
era, Nematodirus and Nematodirella, which are widespread in arctic ungu-
lates and well adapted to life at these latitudes (Tables 2.2, 2.3).
Host and Geographic Distributions. A minimum of nine species of
­nematodirines has been reported in free-ranging arctic ungulates from
North America and Greenland (Table 2.2). There remain some inconsisten-
cies in the definitive identification of species in this group. For example,
Nematodirus archari and N. oiratianus, both species recognized in Eurasia,
have been reported from Dall’s sheep (Nielsen and Neiland, 1974) while
other studies identify N. andersoni and N. oiratianus interruptus in bighorn
and thinhorn sheep of North America, suggesting that the geographic and
host associations for these species be re-evaluated (Lichtenfels and Pilitt,
1983b; Durette-Desset and Samuel, 1989; Rickard and Lichtenfels, 1989).
Similarly, in moose, both Nematodirella alcidis and N. longissemispiculata are
commonly reported across most of this host’s range (reviewed in Fruetel
and Lankester 1988). The latter species probably represents a misidenti-
fication in this host and in most cases is likely N. alcidis (Lichtenfels and
Pilitt, 1983a). Lastly, records of N. helvetianus in muskoxen may be in need
Parasites in Ungulates of Arctic North America and Greenland     129

of examination, assuming that this nematodirine is primarily associated

with domesticated cattle and has been widely transported globally with
their translocation.
Muskoxen have a diverse nematodirine fauna, including those found
in both in moose and caribou, Nematodirella alcidis, N. longissimespiculata
and Nematodirus tarandi, as well as Nematodirella gazelli, and Nematodirus
helvetianus (although see comment above re: N. helvetianus). Absent from
the reported muskox fauna are those species found in Dall’s sheep (N.
oiratianus/O. interruptus, N. spathiger, N. andersoni/archari and N. davtiani).
This may only reflect that muskox populations sympatric with Dall’s
sheep have not been sampled as opposed to a host barrier. Both N. filicol-
lis and N. spathiger, parasites typical of domestic sheep, are reported from
muskoxen sympatric with domestic sheep in Norway (Alendal and Helle,
1983), and it follows that muskoxen are likely suitable hosts for the nema-
todirines in Dall’s sheep.
In contrast to muskoxen, the reported diversity of nematodirines in
caribou and moose is low. For caribou, Nematodirella longissemispiculata
and Nematodirus tarandi are most commonly reported, along with Nema-
todirus skrjabini, which may be a synonym of N. tarandi (Dikmans, 1935a;
Bergstrom, 1983; Lichtenfels and Pilitt, 1983a; Fruetel and Lankester, 1989;
Hoberg et  al., 2001). The low diversity may reflect true species barriers
and/or sampling limited primarily to barren-ground and island cari-
bou populations. The gastrointestinal nematode fauna in the boreal and
mountain woodland caribou ecotypes of the arctic and subarctic is known
only through faecal examinations (Table 2.2) (e.g. Hoar et al., 2009; John-
son et  al., 2010), which have not allowed differentiation among species
of nematodirines. Some of these caribou populations are sympatric with
Dall’s sheep and/or mountain goats and all are likely to have greater sym-
patry with moose than do their barren-ground cousins. Captive caribou
do harbour a greater diversity of nematodirines (Fruetel and Lankester,
1989), supporting the hypothesis that the apparent low diversity in wild
sampled caribou may reflect a combination of ecological isolation and
insufficient sampling.
(b) Ecology. Nematodirines are core components of the ungulate para-
site fauna in arctic and boreal ecosystems in the Holarctic and are well
adapted to the environmental conditions at these latitudes (Hoberg, 2005).
Larvae develop to the infective L3 within eggs. These eggs are resistant
to extreme freezing events, freeze–thaw cycles and desiccation, but direct
sunlight and high temperatures may be detrimental (Marquardt et  al.,
1959; van Dijk and Morgan, 2008).
Nematodirella alcidis is common in moose from temperate regions but
its abundance and distribution in the Arctic and Subarctic are not well
described. In temperate regions, prevalence ranges from 47 to 100% and
infection intensity is typically quite low (Fruetel and Lankester, 1988).
130     Susan J. Kutz et al.

In northwestern Ontario, 19 of 20 moose were infected with N. alcidis

with an average infection intensity of 111 ± 54. Regardless of the time of
year sampled, only 21% of the N. alcidis population were mature adults
and a large proportion of the remaining specimens were ‘short’ L4. The
authors suggested that this may indicate arrested development for this
species where inhibited larvae may serve as a reservoir to replace adult
nematodes and ensure that eggs are produced throughout the year
(Fruetel and Lankester, 1988). In this and other studies, there was no dif-
ference between adult and young moose with respect to prevalence or
intensity of infection. This pattern is in contrast to that of N. longissemi-
spiculata in caribou where large numbers of nematodes, the majority of
which are sexually mature, are found in the duodenum of calves in their
first summer. Calves produce eggs through the winter and are free of
infection the following spring (Fruetel, 1987). Infection of adult caribou
with N. longissemispiculata is rare, although it is seen in males during the
rut. Additionally, nematodirine eggs were common in approximately
50% of adult female caribou of the Kangerlussuaq-Sisimiut herd of west
Greenland but have not been identified to species (Steele et al., 2012).
Eggs and infective larvae of N. alcidis and N. longissemispiculata can sur-
vive freezing and desiccation and may live for extended periods in the
environment (Fruetel, 1987) (Fruetel and Lankester, 1988). In muskoxen,
adult animals commonly shed eggs of Nematodirines and egg produc-
tion tends to increase in the summer and drop off in the fall (Samuel and
Gray, 1974) (Table 2.3).
Observations on larval development for Nematodirus spp. in domes-
tic animals provide some additional insights into the ecology of these
parasites. Hatching of nematodirines occurs within a temperature range
specific to the species (11–17°C for N. battus but 6–20°C for N. filicol-
lis) and, depending on species and geographic location, chilling may be
important to trigger hatching. For example, for N. battus, the proportion
of eggs that hatch without chilling (i.e. in the fall) decreases at more
northern latitudes (van Dijk and Morgan, 2008; van Dijk and Morgan,
2010). In the Arctic, it is hypothesized that hatching of nematodirines
should be triggered by an extended period of chilling (i.e. the winter)
as opposed to no chilling (i.e. hatching in the summer/fall) (van Dijk
and Morgan, 2010). Hatching after chilling would synchronize appear-
ance of the majority of the L3 in the spring and allow for transmission
throughout the short arctic summer. This strategy may be better than fall
hatching for two reasons: 1) the survival of L3 that hatch after chilling is
greater than those that have not been chilled (i.e. fall) (van Dijk and Mor-
gan, 2010) and 2) L3 hatching from eggs at the end of a short arctic sum-
mer would have a very narrow window for transmission and may not
survive the subzero winter temperatures (van Dijk and Morgan, 2010).
However, in southern Greenland, Nematodirus spp. of sheep, including
Parasites in Ungulates of Arctic North America and Greenland     131

N. spathiger, N. helvetianus and N. abnormalis, may hatch within a month

of deposition in the first summer. Development and hatching in this
environment is not synchronous and may extend over 37 months (Rose
and Jacobs, 1990). Although at high latitude, coastal southern Greenland
has a relatively mild maritime climate and the epidemiology of parasites
in this environment may not reflect what occurs in a more ‘arctic’-type
Differences in development and hatching strategies among Nematodi-
rus species infecting a single host may provide a competitive advantage
of one species over another depending on ambient conditions (van Dijk
et al., 2009) and may partition parasite species over time and space. Those
with a lower hatching threshold may be available to infect hosts earlier in
the spring while those with a higher hatching threshold may not be avail-
able until later in the summer. For example, the developmental threshold
for N. helvetianus is 3°C whereas development for N. spathiger does not
occur below 6–7°C (Rose and Jacobs, 1990). Understanding development
thresholds and ranges, as well as triggers for hatching, is important as
these are key factors influencing the timing and intensity of host exposure
and, consequently, the timing and severity of disease. Additionally, such
information is essential to understand individual species responses to cli-
matic conditions and climate change.
(c) Impact. Nematodirus spp. can cause significant disease in domestic
livestock, particularly young animals (Samizadeh-Yazd and Todd, 1979
), but little is known about the impacts of this group of nematodes in
arctic ungulates. Nematodirella longissemispiculata was reported from the
duodenum and anterior jejunum of a wild muskox and was associated
with enteritis characterized by ‘petechial haemorrhages, some denuding of the
mucosa and a quantity of mucus in the lumen. In addition reddish plaque-like
areas were observed on the walls of the duodenum in the area where these worms
were found. Microscopic examination…presence of a granulomatous-type lesion’
(Gibbs and Tener, 1958). In caribou, pathology caused by this species is
likely limited to calves (Fruetel, 1987). High infection intensities with N.
helvetianus, N. longissemispiculata, and other gastrointestinal nematodes
in captive muskoxen in Norway were considered, along with other para-
sites, as a possible cause of the poor body condition of animals on the
farm (Alendal and Helle, 1983). Nematodirella alcidis in moose is reported
from the anterior third of the small intestine but pathology and clinical
disease in this host are not known (Threlfall, 1967; Fruetel and Lankester,
1988). In Dall’s sheep, Nematodirus species may be partitioned in the small
intestine (Nielsen and Neiland, 1974) and species-specific differences in
impacts might be expected. Data collected from Dall’s sheep in the Mack-
enzie Mountains, NT, in 1971–1972 suggest a trend for higher infection
intensities with Nematodirus spp. in non-pregnant compared to pregnant
132     Susan J. Kutz et al.

ewes and in ewes in poor body condition compared to those in very good
condition (Simmons et al., 2001). Subfamily Oxyurinae Skrjabinema spp.

(a) Host and Geographic Distributions. Species of Skrjabinema are pinworms
of the large intestine and caecum. Based on faecal and post-mortem
examinations, Skrjabinema spp. are present at low to moderate prevalence
and intensity in Dall’s sheep and mountain goats, are rare in caribou and
absent from moose and muskoxen (Tables 2.2 and 2.3) (Cowan, 1951; Kerr
and Holmes, 1966; Samuel et al., 1977; Simmons et al., 2001). Skrjabinema
ovis is common in Dall’s sheep and infection intensities are generally low,
ranging from 1 to 60+ worms (Nielsen and Neiland, 1974; Simmons et al.,
2001). Skrjabinema may be underdiagnosed in arctic ungulates as egg shed-
ding can be low and intermittent and few parasitological studies have
included thorough examinations of the large intestines and caecum.
(b) Ecology. Oxyurids are directly transmitted parasites. In most host
species, gravid females migrate to the anus of the host and deposit eggs
in the perianal region whence the eggs can be shed in the faeces or, once
infective, can be transmitted directly between hosts. Development to the
infective stage is species dependent and can take hours to days.
(c) Impacts. The Oxyuridae in domestic ungulates are believed to be
generally benign with few symptoms (Bowman et  al., 2003), but their
effects in free-ranging species remain unexplored. Subfamily Trichurinae Trichuris spp.

(a) Host and Geographic Distributions. Species of Trichuris are extremely
uncommon in free-ranging caribou and muskoxen but are found in almost
all surveyed populations of Dall’s sheep (Nielsen and Neiland, 1974; Sim-
mons et al., 2001) (Tables 2.1 and 2.2). The species present in Dall’s sheep is
believed to be T. schumakovitschi. In faecal surveys of Canadian muskoxen,
Trichuris spp. were found at a low prevalence on the mainland but were
completely absent from over 1000 faecal samples examined from Banks
Island, NT (Table 2.2). Interestingly, Capillaria sp., a parasite common in
reindeer in the Palaearctic (Hrabok et al., 2006a), is absent from sampled
populations of free-ranging caribou and muskoxen in North America and
Greenland (Table 2.3) although it was detected in a captive herd of rein-
deer in Alberta (S. Kutz, unpubl. data).
(b) Life Cycle. Trichuris spp. are directly transmitted nematode para-
sites of the large intestine and caecum. The L1 is the infective stage and
Parasites in Ungulates of Arctic North America and Greenland     133

remains within the egg, which is extremely resistant to environmental

conditions. This resistance, particularly to desiccation, may be one of the
factors allowing these parasites to survive in the Arctic.
(c) Impacts. The effects of Trichuris spp. infections on free-ranging arctic
ungulates are not known but low-intensity trichurid infections in captive
muskox calves are often associated with diarrhoea (Seidel and Rowell,
1996). Emerging issues and knowledge gaps

The gastrointestinal nematode fauna of arctic ungulates is generally sparse
with the most species diversity represented by the nematodirines, parasites
well adapted to arctic climates. In recent years, considerable progress has
been made in defining the diversity and host and geographic ranges of the
Trichostrongylina in the arctic ungulates of North America, although much
remains to be done. Fundamental to this progress is recognition of cryptic
species complexes (e.g. T. boreoarcticus and Marshallagia spp.) and the use
of integrated methods that combine diagnostic morphological characters
and DNA-based analyses to develop and refine descriptions and phylog-
enies. Importantly, archived specimens deposited in museum collections
(e.g. Nematodirella, Teladorsagia) have aided in confirming or re-determining
the identity of several species, as well as confirming the presence of cryptic
species (Lichtenfels and Pilitt, 1983a; Hoberg et al., 1999). These collections
are particularly relevant for arctic parasites because of the cost and logistics
of collecting material in the field and the challenges of obtaining specimens
from host species that have become endangered or threatened.
Overall, the trichostrongyline parasites in arctic ungulates appear to
have broad host ranges but there are host-specific patterns of abundance.
For the nematodirines in particular, the role of host species barriers ver-
sus ecological barriers to infection requires further investigation. Examin-
ing the patterns of host and geographic distribution, and perturbations
of these patterns, may provide novel insights into mechanisms of para-
site invasion and establishment (Hoberg et  al., 2012). For example, the
presence of large numbers of ‘strongyle’ type eggs in Dall’s sheep in the
Richardson Mountains is unusual and may reflect the unique interactions
of sheep with muskoxen and caribou in this region. The absence of O.
gruehneri, the most common abomasal parasite of Rangifer, from caribou
colonizing parts of Greenland is particularly surprising and may reflect
unique patterns of host and parasite dispersal into these regions, includ-
ing severe host, and perhaps parasite, bottlenecks. Further exploration of
animal movements, natural and anthropogenic, ecological and species
barriers and successes and failures of parasite colonization events will
contribute to theory on parasite invasion and establishment and provide
134     Susan J. Kutz et al.

insight into the potential for new parasite invasions in the Arctic (Hoberg,
2010; Hoberg et al., 2012).
Transmission dynamics of gastrointestinal nematodes will be influ-
enced by the rapidly changing arctic environment (Hoberg et al., 2008b;
Kutz et al., 2009a,b). In general, warmer and longer summers are antici-
pated to facilitate parasite development and transmission, whereas
extreme temperatures may have negative impacts (Kutz et al., 2009b; Hoar
et al., 2012b). The effects of changing winter conditions are currently spec-
ulative – shorter winters may decrease propensity for larval inhibition,
increased snow cover that insulates parasites may improve parasite sur-
vival whereas increased freeze–thaw cycles will reduce parasite survival.
Some endemic parasites may be better equipped to cope and take advan-
tage of changing conditions (e.g. nematodirines), whereas others (perhaps
ostertagiines) may not.
There is growing evidence that, at least for some species, the free-liv-
ing stages of parasites in the North may have sufficiently broad thermal
tolerances (e.g. O. gruehneri) and/or flexibility in development strategies
(e.g. nematodirines and O. gruehneri) to persist under these changing con-
ditions (van Dijk and Morgan, 2010; Hoar et al., 2012b). Larval inhibition
within the host and overwintering of eggs and larvae in the environment
are important strategies for overcoming adverse environmental condi-
tions and can synchronize parasite development with the availability of
susceptible hosts, such as spring-borne young (Eysker, 1993; Sommerville
and Davey, 2002; Cattadori et al., 2005). The different propensity for larval
inhibition in O. gruehneri across its geographic range and in different sub-
species of Rangifer likely reflects selective strategies associated with cli-
matic conditions and host behaviours (Hoar et al., 2012a). Such plasticity
within the species may allow it to maximize its fitness (i.e. transmission)
under a variety of climatic conditions.
Similarly, research on species of Nematodirus in domestic livestock
suggests that selection can drive adaptations in patterns of egg hatching
under different climatic or latitudinal gradients (van Dijk and Morgan,
2010) such that these nematodes may be very well equipped to survive
climate change in the Arctic. The nematodirines are a core, diverse and
neglected yet potentially pathogenic component of the gastrointestinal
parasite fauna of arctic ungulates. An understanding the ecology of these
parasites under the current climate warming conditions is of considerable
importance for the health of arctic ungulates and may provide a novel
insight into the epidemiology of nematodirines in domestic species. These
arctic species remain essentially untouched by the selection pressures of
the livestock production industry and may provide a simpler model for
exploring concepts of importance for nematodirines of domestic host spe-
Parasites in Ungulates of Arctic North America and Greenland     135

Invasions of new hosts or parasites to the Arctic may result from a

variety of factors including natural range expansion through gradual
movements or stochastic events, translocation associated with agriculture
or conservation efforts, or anthropogenic change including climate and
landscape perturbation (Kutz et  al., 2009b; Hoberg, 2010; Hoberg et  al.,
2012). The gastrointestinal nematode fauna of temperate free-ranging
ungulate species in Canada is considerably more diverse than that of arc-
tic ungulates, the former consisting of a mosaic of endemic and introduced
parasites (Table 2.4) (Hoberg et  al., 2001,2008a; deBruyn, 2010). There is
evidence that, given appropriate conditions, some of these species may
be able to invade and persist in high latitude ecosystems (e.g. Waller and
Chandrawathani, 2005; deBruyn, 2010).
Trichostrongylus axei is one such parasite that may have already estab-
lished successfully at arctic latitudes. Trichostrongylus axei is not known
as part of the typical endemic fauna of arctic ungulates in North America
or Greenland but it has been reported from a variety of arctic ungulates
in captivity at southern latitudes and in Fennoscandia, as well as in
domestic sheep in Greenland (Alendal and Helle, 1983; Rose et al., 1984;
Bye, 1987; Bye et al., 1987; Fruetel and Lankester, 1989). It was recently
found in an introduced population of elk in the Yukon (deBruyn, 2010).
Although the original source of T. axei in this population is not known
(i.e. introduced or naturally present in endemic YT ungulates), its pres-
ence in the elk years after their translocation indicates that it is currently
able to circulate in this northern environment. It is a host generalist
and likely to spill-over to moose and caribou in the region, if it has not
A second genus of considerable concern is Haemonchus. Some species
of Haemonchus are pathogenic abomasal nematodes of domestic sheep and
cattle that can spill-over into wild ungulates and cause significant disease
(Hoberg et al., 2004). Both H. contortus and H. placei have been reported
in wild deer from western Canada (Table 2.4)(deBruyn, 2010). Species of
Haemonchus and H. contortus are considered tropical parasites and the
free-living stages are susceptible to both cold and dry conditions and
require a mean monthly temperature of 18°C to persist (Gordon, 1948;
Hoberg et al., 2004). These attributes may explain the absence of endemic
species in North America and current geographic limits of introduced
species in the boreal and temperate zones (Hoberg et al., 2012c). Thus, the
establishment of H. contortus above the Arctic Circle in Sweden is unusual,
although these populations are limited to domestic sheep under intense
management and confinement (Waller and Chandrawathani, 2005). A
high propensity for larval inhibition in the abomasal mucosa, in con-
junction with animal husbandry practices, appear to be key features that
allow it to persist in domestic livestock at these latitudes (Waller et al.,
2004). Semi-domesticated reindeer in Finland have been experimentally
Susan J. Kutz et al.
TABLE 2.4  Some gastrointestinal nematode species reported from cervids in western Canada. Adapted from deBruyn (2010)

Parasitee Woodland caribou Mule deer White-tailed deer Black-tailed deer Elk Moose

Haemonchus contortus ABf
Heamonchus placei AB, SK
Marshallagia marshalli AB AB
Mazamastrongylus odocoilei SK AB, SK
Orloffia bisonis (Syn. Ostertagia bisonis) ABa ABa
Ostertagia gruehneri/O. arctica AB, BC
Ostertagia mossi/O. dikmansi SK
Ostertagia ostertagi ABa ABa
Ostertagia sp. ABb
Spiculopteragia boehmi AB AB AB
Teladorsagia boreoarcticus AB, BC
Teladorsagia circumcincta BC AB, BCa,d
Trichostrongylus axei ABa ABb
Small intestine
Cooperia oncophora (Syn. C. surnabada) AB, ABa ABb
Nematodirella alcidis ABb ABb
Nematodirella longissimespiculata ABc
Nematodirus helvetianus AB, ABa ABb
Nematodirus odocoilei AB, BC AB, BCa,d
Nematodirus spathiger AB
Skrjabinema ABb
Trichostrongylus colubriformis AB
Trichostrongylus longispicularis ABb
a  Stock (1978).
b  Stock and Barrett (1983).

Parasites in Ungulates of Arctic North America and Greenland    

c  Samuel et al. (1976).

d  Walker and Becklund (1970).

e  Among the Ostertagiinae, only names for the major morphotype for polymorphic species are included.

f AB = Alberta, BC = British Columbia, SK = Saskatchewan.

Records are from DeBruyn (2010) unless otherwise indicated.

138     Susan J. Kutz et al.

infected with H. contortus (Hrabok et al., 2006b) and Haemonchus sp. has
also caused acute disease and death of muskoxen in captivity (Durrell
and Bolton 1957) (MacDonald et  al., 1976). The absence of H. contortus
in Greenland sheep may suggest that it was not present in the original
sheep brought to Greenland in 1906 and 1915 from the Faroe Islands and
Iceland (Rose et al., 1984). The fact that Haemonchus is currently absent
from Iceland sheep supports this contention (Gudmundsdottir, 2006).
Whether Haemonchus spp., if introduced, could be maintained in the Arc-
tic by populations of wild ungulates in the absence of domestic livestock
or confinement farming is unknown. If established at arctic latitudes,
Haemonchus could become a serious cause of morbidity and mortality in
wild ungulates.
Spiculopteragia boehmi is another potentially pathogenic, invasive para-
site of note. It is a Eurasian abomasal nematode of red deer that was trans-
located to North America (and globally) and is now found in wild deer
and elk in geographically disjunct regions of western Canada and the USA
(deBruyn, 2010; Rickard et al., 1993). Spiculopteragia is well established in
game ranched reindeer, and probably elk (C. elaphus), in western Canada
and appears to have significant impacts on body condition of these ani-
mals (S. Kutz, unpubl. obs). Range expansion into temperate caribou
populations is expected but establishment at arctic latitudes is uncertain
(deBruyn, 2010).
Gastrointestinal nematodes are well established as production limit-
ing parasites in domestic species and are increasingly recognized as hav-
ing a role in the health and population dynamics of free-ranging hosts
(Hudson and Greenman, 1998; Hudson et  al., 1998; Albon et  al., 2002).
While our knowledge of the diversity of gastrointestinal nematodes of
arctic ungulates has improved substantially, our knowledge of the ecol-
ogy and impacts of this group of parasites remains superficial for almost
all species except O. gruehneri. For some of these parasites, even the very
basics of the life cycle remain unknown. For the rest, knowledge of the
life cycle and potential impacts is limited to what has been learned from
a few pilot studies or extrapolated from related parasites of domestic
As parasites with considerable plasticity and resilience in their
responses to climatic conditions, some gastrointestinal nematodes of arc-
tic ungulates are likely to continue to thrive under ongoing climate change
(e.g. Nematodirines, Marshallagia), while others may not be as success-
ful (e.g. Teladorsagia, Ostertagia). The transmission dynamics and relative
abundance and impacts of these parasites will be sensitive to shifts in
diversity, abundance and behaviour of host communities, as well as to
invasions of new hosts and parasites. Extirpation of endemic faunas may
be a result of competition with such invasive parasites. Parasite-mediated
competition among hosts may also occur. A knowledge of how historical
Parasites in Ungulates of Arctic North America and Greenland     139

ecological conditions have structured the parasite communities and how

parasites currently circulate among hosts will allow us to anticipate how
these communities may respond to invasions of southern hosts and para-
sites and ultimately how that will influence the health and sustainability
of wildlife populations.

2.3.2. Lung and tissue nematodes: Protostrongylidae and

The Protostrongylidae are pathogenic nematodes of free-ranging and
domestic ungulates and lagomorphs around the world. Higher taxonomy
for this group was established by Boev (1975), Kontrimavichus et al. (1976)
and Carreno and Hoberg (1999). Species of four subfamilies are known
in ungulates across North America (Fig. 2.7). Those that live as adults in
the lungs belong to the subfamilies Muelleriinae, Protostrongylinae and
Varestrongylinae, and those that live as adults in the skeletal muscles or
central nervous system are referred to the Elaphostrongylinae. At high
latitudes of Canada and AK, various protostrongylid species occur in bar-
ren-ground, Grant’s, and woodland caribou, thinhorn sheep, moose, mus-
koxen, and mountain goats (Table 2.5). Protostrongylids have not been
reported from caribou or muskoxen in Greenland; however, Muellerius
sp. (Muelleriinae) is reported from domestic sheep in southern Greenland
(Rose et al., 1984). Parasite species diversity, prevalence, and abundance
vary with host and geographic location.
Among protostrongylid species with lung-dwelling adults, eggs pro-
duced by the females hatch to release first-stage larvae (L1) that move up

FIGURE 2.7  Tissue and lung Strongylida reported from ungulates of arctic North
America, including Greenland.
140     Susan J. Kutz et al.

TABLE 2.5  Tissue and blood nematodes reported from ungulates of arctic North Amer-
ica, including Greenland. Data compiled from available published and grey literature

Host and parasite species State/ province Herd, region or nearest place name

Parelaphostrongylus AK Mulchatnaa; Northern Alaska Penin-
andersoni sulaa
YT Porcupinea; Chisanaa
NT Cape Bathursta; Tsiigehtchica; Blue-
nose Westa; Beverlyb
QC/NL Rivière-aux-Feuillesc; Rivière
Georgea,b; Mealy Mountainsa
Parelaphostrongylus NT Hay Riverd
Varestrongylus sp. n. AK Northern Alaska Peninsula, Mulchatnaa
YT Porcupinea
NT Beverlya; Bluenose Easta; Cape
Bathursta; Godlin Lakesa
NL Mealy Mountainsa
Dictyocaulus eckertiae AK Western Arctic, Northern Alaska Pen-
insula and Kenai Peninsulam
QC/NL Rivière Georgee
GL AM herdf
Onchocerca cervipedis AK Mulchatnag
Setaria yehi AK College and Cantwellh (in reindeer,
originally from Nome)
NT Not specifiedi
Dall’s sheep
Parelaphostrongylus AK Central Alaska Ranged; Chugach
odocoilei Mountainsd; Wrangel Mountainsd
YT Farod; Kluane National Parkd; St. Elias
NT Mackenzie Mountainsd,j
Protostrongylus stilesi AK Alaska Ranged,k; Baird Rangel; Brooks
Rangel; Chugach Mountainsl; Wran-
gel Mountainsd
YT Anvil Mountainsd; Ivaavik National
Parkd; St. Elias Mountainsd
NT Mackenzie Mountainsd,j
Varestrongylus sp. n. AK Tlikakila River, Lake Clark National
Parasites in Ungulates of Arctic North America and Greenland     141

TABLE 2.5  (continued)

Host and parasite species State/ province Herd, region or nearest place name
Dictyocaulus eckerti AK Palmerm
Onchocerca cervipedis AK Tok Rivern; Palmern
YT Variouso
NT Mackenzie Mountains, Mackenzie
Valley p
Setaria yehi AK Unspecifiedi; Fairbanksq; Delta Junc-
Rumenfilaria andersoni AK Interior including Fairbanks, Tanana
Flats, Kuskokwim River, Seward
Umingmakstrongylus pal- NT Sahtu Settlement Regionr
likuukensis NU West of Kugluktuks,t; Victoria Island
(Lady Franklin Point) u
Varestrongylus sp. n. YT Firth Riverk
NT Aklavika
NU Cambridge Bay v; Thelon Game Sanc-
Protostrongylus stilesi AK Eastern North Slopew
YT Northern Yukon x
NT Big Fish River (near Aklavik)y
Dictyocaulus eckerti NU Kitikmeot region z
QC Kuujjuaqaa
Dictyocaulus AK Eastern North Slopew
NT Banks Islandab
NU Bathurst Islandac; Thelonad
a  Kutz et al. (2007). p  S. Kutz, C. Tobac, G. Verocai (unpubl. obs.).
b  Lankester and Hauta (1989). q  Quist and Beckmen (2011).
c  Asmundson and Hoberg (pers. comm.). r  S. Kutz, A. Veitch, R. Popko (unpubl. data).

d  Jenkins et al. (2005a). s  Gunn and Wobeser (1993).

e  Fruetel and Lankester (1989). t  Hoberg et al. (1995).

f  C. Cuyler, R. White, S. Kutz (unpubl. data). u  S. Kutz, K. Orsel, G. Verocai (unpubl. obs.).

g G. Verocai, K. Beckmen(i), Hoberg v  G. Verocai, S. Kutz, S. Checkley (unpubl. data.).

(unpubl. data). w  Afema (2008).

h  Dieterich and Luick, (1971). x  S. Kutz (unpubl. data).

i  Becklund and Walker (1969). y  Hoberg et al., (2001).

j  Kutz et al. (2001d). z  Hoglund et al. (2003).

k  Neiland (1972). aa  USNPC, 2011.

l  Jenkins et al. (2007). ab  M. Branigan (unpubl. data).

m  K. Beckmen (unpubl. data). ac  Gibbs and Tener (1958).

n  K. Beckmen, G. Verocai, E. Hoberg (unpubl. data). ad  Samuel and Gray (1974).

o  P. Merchant (pers. comm). ae  Reported as D. viviparus but most likely D. eckerti.
142     Susan J. Kutz et al.

the respiratory tree, are swallowed and passed in the faeces. The adults
of tissue-dwelling species (Elaphostrongylinae) produce eggs that are
deposited in the blood stream and transported to the pulmonary vas-
culature where hatching releases the L1. These migrate into the alveoli,
then follow the same route as larvae of the lung-dwelling species and are
passed in the faeces. First-stage larvae of genera within the Muelleriinae,
Elaphostrongylinae and Varestrongylinae have kinked tails with small
dorsal spines (dorsal-spined larvae – DSL). It is not possible to reliably
differentiate among these genera on the basis of larval morphology alone
(Hoberg et al., 2005); therefore, DNA-based methodologies are required
for definitive identification (Huby-Chilton et al., 2006; Kutz et al., 2007).
The L1 of the Protostrongylinae have straight spike tails, lack dorsal
spines and also cannot be reliably distinguished morphologically at
either the generic or species level (e.g. Boev, 1975). In general, L1 of north-
ern protostrongylids can survive well in the often-harsh external environ-
ment and are characterized by a degree of freeze tolerance but repeated
freeze–thaw cycles, shifts in humidity and exposure to high temperatures
will reduce viability (Forrester and Lankester, 1998; Shostak and Samuel,
1984; Lorentzen and Halvorsen, 1986).
Gastropod intermediate hosts, which are invaded by L1 from ungu-
late faeces, are required for continuation of the life cycle for all Proto-
strongylidae (Anderson, 2000). Development to the infective third-stage
larvae (L3) is completed through a variety of terrestrial and aquatic
gastropod species, but there is a certain degree of host specificity. Lar-
val development rates and success within the intermediate host vary
depending on both parasite and gastropod species and are temperature
dependent. Mammalian hosts become infected when they ingest gas-
tropods harbouring L3 or L3 that have spontaneously emerged from
the gastropods and are present in the environment (Anderson, 2000;
Kutz et al., 2000b).
Adults, eggs and L1 of lung-dwelling species and eggs and L1 of tissue-
dwelling species can cause significant pulmonary damage, notably local-
ized or multifocal granulomatous pneumonia. Moreover, the developing
larvae and adults of species of the Elaphostrongylinae can cause myositis
and neurological disease, with particularly severe disease in ‘aberrant’
host species (Anderson, 2000; Lankester, 2001; Jenkins et al., 2005b). Subfamily Protostrongylinae

The Protostrongylinae is a diverse group of parasites with a cosmopolitan
distribution in ungulates and lagomorphs, although the greatest diver-
sity is seen in Eurasia (Boev, 1975). Several species have been reported in
cervids and bovids from North America, including Orthostrongylus mac-
rotis in mule deer, Protostrongylus frosti in bighorn sheep and P. coburni in
Parasites in Ungulates of Arctic North America and Greenland     143

white-tailed deer from northeastern USA (Dikmans, 1935b); only P. stilesi

and P. rushi are present in arctic and subarctic regions. Protostrongylus stilesi

Protostrongylus stilesi is a small (males 17.55–20.79mm in length, female
length not established) (Hoberg et al., 2002) and slender lung nematode
found in the lung parenchyma of wild sheep and mountain goats from
North America.
(a) Host and Geographic Distributions. Protostrongylus stilesi is common
in bighorn (Ovis canadensis), Stone’s and Dall’s sheep and mountain goats,
across their ranges (Neiland, 1972; Uhazy et al., 1973; Pybus et al., 1984;
Kutz et al., 2001d; Jenkins et al., 2005a). Based on post-mortem examina-
tions together with faecal surveys where L1 were presumed to be P. stilesi
(P. rushi, although less likely, was not ruled out), prevalence ranges from
50 to 100% in thinhorn sheep herds and 50 to 78% in mountain goat herds
(Jenkins et al., 2006b).
Protostrongylus stilesi is also present at low intensities in an introduced
population of muskoxen (O. m. wardi) that are sympatric with Dall’s sheep
in northern YT and northwestern NT (Hoberg et al., 2002), and L1 typical
of Protostrongylus sp. are present in introduced muskoxen that are sym-
patric with Dall’s sheep in western AK (L. Adams, K. Beckmen, unpubl.
obs.). The occurrence of P. stilesi in muskoxen is considered a recent host
switch associated with anthropogenic breakdown of ecological barriers in
conjunction with climate change (Hoberg et al., 2002). Following histori-
cal extirpation, muskoxen were introduced to the Arctic Coastal Plain of
AK in the late 20th century. Later expansion of this population to the east
along the northern shoulder of the Brooks Range has resulted in intermit-
tent sympatry with Dall’s sheep and consequent infection with P. stilesi.
Although infections in muskoxen become patent, larval shedding is low
and it is unknown whether P. stilesi would be maintained in the absence of
Dall’s sheep (Hoberg et al., 2002; Kutz et al., 2004b).
(b) Ecology. The life cycle of P. stilesi is similar to other pulmonary
protostrongylids. Larvae of bighorn sheep origin developed to L3 within
11–60 days in several gastropod genera, including Pupilla, Vallonia, and
Vertigo (Pillmore, 1956; Monson and Post, 1972) and those of Dall’s sheep
origin developed to L3 within 34 days in experimentally infected wild-
caught pupillid snails (Vertigo and Columella spp.) at room temperature
(mean 22°C) (E. Jenkins and J. Skific pers. comm.). Emergence of small
numbers of L3 from gastropod intermediate hosts occurs and although
it is not considered an important feature of the parasite’s epidemiology
in bighorn sheep (Monson and Post, 1972), it may be more important in
the Arctic, extending transmission into winter. Third- and fourth-stage
larvae have been recovered from foetuses and neonatal bighorn lambs,
144     Susan J. Kutz et al.

suggesting that transplacental transmission occurs (Forrester and Senger,

1964; Hibler et al., 1972). The prepatent period in a single experimentally
infected Dall’s sheep was 45 days (E. Jenkins and J. Skific pers. comm.)
and the finding of P. stilesi adults in Dall’s lambs as young as two months
suggests either infection very early in life or that transplacental transmis-
sion might also occur in thinhorn sheep (Jenkins et al., 2007). First-stage
protostrongylid larvae, not identified to subfamily, were also observed in
the bronchi of a wild Dall’s foetus from AK at the end of April (K. Beck-
men, K. Burek, unpubl. obs.). These may be a result of haematogeneous
spread of L1 from the dam, which is unlikely in the case of the Protostron-
gylinae but perhaps more likely for Parelaphostrongylus odocoilei or a patent
infection with species of either genus.
In Dall’s sheep in the Mackenzie Mountains, NT, larval production
tends to be seasonal, with prevalence lowest in August and increasing
through the fall and intensity also increasing through fall and winter and
peaking in the spring (annual range of 32–1075 LPG) (Jenkins et al., 2006b).
Development and transmission of P. stilesi under arctic conditions have
not been investigated in any detail; however, using a degree–day model
for protostrongylid development (Kutz et al., 2002), Jenkins et al. (2005b)
suggested that L3 might not develop in a single summer at arctic latitudes.
The authors hypothesized that freeze tolerance of L1, overwintering of
larvae in gastropods, transplacental transmission and L3 emergence may
all contribute to the persistence of this parasite at arctic latitudes (Jenkins
et al., 2006b).
(c) Impacts. In naturally infected Dall’s sheep, P. stilesi can cause severe
verminous lesions in the lung parenchyma associated with adults, larvae
and eggs. Grossly, there are firm, pale, coalescing lesions of 5–70mm in
diameter primarily along the caudodorsal border of the diaphragmatic
lobe, but also in other lobes, and it is estimated that, in heavy infections,
up to 36% of the lung volume can be compromised (Neiland, 1972; Kutz
et al., 2001d). Histologically, there are focal aggregations of inflammatory
cells surrounding adult nematodes and immature stages, as well as fibro-
sis, bronchiolar hyperplasia and mild fibrino-haemorrhagic exudate (Kutz
et al., 2001d). In muskoxen, lesions are located in the caudodorsal and dia-
phragmatic surfaces of diaphragmatic lobes, are round to oval (3–5mm),
tan to red brown, extending into the lung parenchyma and contain adults,
ova and larvae of the parasite. Histologically, adults are confined to alveo-
lar parenchyma and surrounded by mild to focally marked lymphocyte/
macrophage infiltrate (Hoberg et al., 2002). Pathology is not described in
mountain goats.
The effects of P. stilesi in Dall’s sheep at a population level remain
unknown. Historically, P. stilesi was considered an important pathogen in
bighorn sheep and linked to the lungworm–pneumonia complex. Subse-
quent studies suggest, however, that while lungworms might predispose
Parasites in Ungulates of Arctic North America and Greenland     145

to other pneumonias, their effects on the individuals and populations of

this host species may be more subtle and indirect (Festa-Bianchet, 1991).
Of possible significance with respect to Dall’s sheep is that, across their
central and southern range, they may be co-infected with the muscleworm
P. odocoilei. Eggs and larvae of P. odocoilei cause significant pulmonary
damage and co-infections could result in additive or synergistic pulmo-
nary damage (Kutz et al., 2001d; Jenkins et al., 2007). Protostrongylus rushi

Adults of P. rushi are larger (males 18–32mm, females about 38mm in
length) than P. stilesi and are found in the trachea, bronchi, and larger bron-
chioles. Protostrongylus rushi has been reported in a Dall’s sheep from the
YT based on a single museum specimen (CMNP 1988-0522) (Kutz et al.,
2001d) and in mountain goats at Mt. Juneau and adjacent to Haines, AK
(USNPC 100426, 105139). It also occurs in bighorn sheep from the Cana-
dian Rocky Mountains (Uhazy et al., 1973) and mountain goats from cen-
tral BC (Jenkins et al., 2004). However, the true geographic range of this
parasite in the Arctic remains unknown. Although adults of P. stilesi and
P. rushi are easily differentiated, the L1 are morphologically very similar
and require DNA-based analyses for identification (e.g. Kutz et al., 2007).
Further survey and inventory are necessary to determine the geographic
distribution of P. rushi in Dall’s sheep and mountain goats and its potential
significance in these caprines. Subfamily Muelleriinae

Members of the Muelleriinae are a monophyletic group of typically cyst-
forming lungworms of the Caprinae and include the genera Muellerius,
Cystocaulus, and Umingmakstrongylus (Carreno and Hoberg, 1999). Uming-
makstrongylus pallikuukensis is the only species of the subfamily endemic to
North America. Muellerius capillaris is a cosmopolitan parasite of domes-
tic sheep and goats that was introduced to North America with domestic
livestock (Anderson, 2000) and has since spilled over to bighorn sheep
(Pybus and Shave, 1984; Ezenwa et al., 2010). Species of Cystocaulus have
distributions in Eurasia and although this genus is the sister of Umingmak-
strongylus, it has not been reported in North America. Umingmakstrongylus pallikuukensis

Umingmakstrongylus pallikuukensis is a large (males up to 22cm and females
to 65cm long), cyst-forming, pulmonary nematode specific to muskoxen
(Kutz et al., 1999). It was first discovered west of Kugluktuk, NU, in 1988
(Gunn and Wobeser, 1993; Hoberg et al., 1995).
146     Susan J. Kutz et al.

(a) Host and Geographic Distributions. In the late 1990s, U. pallikuuken-

sis was present at near 100% prevalence in muskoxen on the western
Canadian mainland between the Mackenzie and Coppermine rivers and,
despite extensive survey, was not found in muskox populations elsewhere
(Gunn and Wobeser, 1993; Hoberg et al., 1995; Kutz, 2000). Recently, it has
been detected on Victoria Island, NU, and east of the Coppermine River,
suggesting significant range expansions (S. Kutz, K. Orsel, M. Dumond,
G. Verocai unpub. obs.). It has not been found in sympatric caribou and
did not establish in experimentally exposed Dall’s/Stone’s sheep hybrids
or domestic sheep (Kutz et al., 1999 ; Kutz et al., 2004a).
(b) Ecology. Umingmakstrongylus pallikuukensis follows a typical proto-
strongylid life cycle with temperature dependent development in gastro-
pod intermediate hosts. In the core of the parasite’s range on the Canadian
mainland, the meadow slug, Deroceras laeve, appears to be the most abun-
dant intermediate host but larvae can also develop to L3 in at least two
(Catinella sp. and Euconulus fulvus) of the five terrestrial species and one
(Aplexa hypnorum) of the four aquatic species present in the area. The lar-
val development period in experimentally exposed D. laeve ranges from 9
days at 23.4°C, to 42 days at 11.5°C (Kutz et al., 2001c; Kutz et al., 2002) and
the prepatent period (PPP) in experimentally infected captive muskoxen
is 91–95 days (Kutz et al., 1999).
Umingmakstrongylus pallikuukensis appears to be an exceptionally well
adapted, single host, arctic parasite: it is large, long lived (at minimum two
years and likely much longer) and highly fecund (up to 3 million L1/day
in experimentally exposed muskoxen with adult parasite burdens similar
to those observed in the field); L1 are resistant to freezing and desicca-
tion and develop rapidly and efficiently in a gastropod intermediate host
species that is relatively abundant and vagile; up to 100% of L3 emerge
from the gastropods suggesting the possibility of year-round transmission
and infection accumulates with age and causes minimal inflammatory
response in muskoxen (Kutz et al., 1999; Kutz, 2000; Kutz et al., 2001b).
Where it is present, prevalence approaches 100% in the affected popu-
lation and calves are infected in their first summer (Gunn and Wobeser,
1993; Kutz et al., 2001b).
The restricted geographic distribution of U. pallikuukensis likely reflects
a history of near extirpation of muskoxen in the early 1900s as well as
limiting historical climatic conditions (Hoberg et al., 1995; Hoberg et al.,
2008a). Empirical models suggest that between 1973 and 2002, concurrent
with regional warming, larval development within the intermediate host
reached a tipping point, shifting from a two- to one-year period. This
shift in development rate would have a considerable influence on infec-
tion pressure and transmission dynamics and range expansion under
the current regime of climate warming was predicted (Kutz et al., 2005).
Consequently, the recent finding of U. pallikuukensis on Victoria Island,
Parasites in Ungulates of Arctic North America and Greenland     147

a large arctic island separated from the mainland by Coronation Gulf,

is a substantial range expansion (Kutz et al., 2009b). A broadened range
reflects a permissive climate, presence of suitable gastropod intermediate
hosts and an event for expansion and establishment most likely medi-
ated through infrequent muskox movement between the mainland and
the island.
(c) Impacts. Adult parasites inhabit spherical to ovoid grey–brown
cysts of up to 4cm in greater diameter, containing up to… 5–7 adult
worms. Cysts are located throughout the lung parenchyma and some are
easily visible and palpable. Histologically, cysts consist of a wall of con-
nective tissue surrounding adult worms, together with numerous eggs,
L1 and amorphous debris (Hoberg et al., 1995; Kutz et al., 1999). Some
cysts are calcified, which is thought to indicate long-standing infection
and some contain no adult parasites. There is little inflammatory reaction
outside the region directly adjacent to the cysts. Cysts appear to accumu-
late with age and naturally infected older bulls may contain up to 250
(Gunn and Wobeser, 1993). On radiographic examination cysts are vis-
ible as opacities and are also clearly evident on computed tomography
(Kutz et al., 1999).
The population-level impacts of an endemic infection with U. palli-
kuukensis, or the introduction to a naive population such as that on Vic-
toria Island, remain poorly understood. There are anecdotal reports of
epistaxis in free-ranging muskoxen that have been stressed by running,
and one infected captive muskox demonstrated epistaxis when restrained
on a bovine examination tilt table. Conceivably, the parasites may have
significant energetic costs for heavily infected muskoxen and the pathol-
ogy may lead to exercise intolerance and increases in susceptibility to
predation. Subfamily Varestrongylinae

The Varestrongylinae is composed of a number of species within the gen-
era Varestrongylus and Pneumostrongylus. These are small lungworms typi-
cally found in the terminal bronchioles of cervids and bovids across the
Holarctic (Boev, 1975). In North America, two species are known, V. alpe-
nae in white-tailed deer and a recently discovered species, Varestrongylus
sp. n., in caribou, muskoxen and moose; only the latter species is reported
from the Arctic (Kutz et al., 2007). Varestrongylus sp. n.

Varestrongylus sp. n. is a miniscule lungworm (1–2cm) found deep in the
airways or parenchyma of the lungs. Taxonomic description of this para-
site is in progress (G. Verocai, E. Hoberg, M. Simard, S. Kutz, unpubl. obs.).
148     Susan J. Kutz et al.

(a) Host and geographic distributions. Varestrongylus sp. n. has a broad

host and geographic range, naturally infecting muskoxen (O. m. moscha-
tus and O. m. wardi), woodland, Grant’s and barren-ground caribou, and
rarely, moose across most of arctic and subarctic North America (Kutz
et al., 2007). Unidentified DSL previously found in woodland caribou in
several Canadian provinces may also be from this species (Lankester et al.,
1976; Gray and Samuel, 1986; Lankester and Fong, 1998; Kutz et al., 2007)
but further investigations are required.
Varestrongylus sp. n. occurs in co-infections with Parelaphostrongylus
andersoni in some barren-ground caribou herds and with P. odocoilei in
woodland caribou from western Canada (Kutz et al., 2007). Co-infections
with P. stilesi in muskoxen are probable (Hoberg et al., 2002; L. Adams, K.
Beckmen, unpubl. obs.), as are co-infections with U. pallikuukensis; how-
ever, the latter would be difficult to detect. The substantial lesions caused
by U. pallikuukensis may obscure the more subtle changes caused by the
Varestrongylus. Similarly, molecular detection based on DSL from faeces
may be confounded by massive larval production from U. pallikuukensis,
which may obscure the less abundant L1 of Varestrongylus (Kutz et  al.,
(b) Ecology: Varestrongylus sp. n. follows the typical protostrongylid life
cycle. It was found in a naturally infected slug, Deroceras laeve, from the
NT (Kutz et al., 2007) and in preliminary studies developed to L3 in both
D. laeve and Deroceras reticulatum (G. Verocai, S. Kutz unpubl. obs.). The
prepatent period, pathology and impacts of this parasite in its hosts are
not known: gross lesions have not been observed in lungs from a small
number of naturally infected muskoxen and caribou (G. Verocai, S. Kutz
and M. Simard unpubl. obs.). Subfamily Elaphostrongylinae

The Elaphostrongylinae consist of two genera with a minimum of six
species, two of which occur in arctic ungulates of North America. Spe-
cies of the genus Parelaphostrongylus are native to North America whereas
Elaphostrongylus is a Palaearctic genus. A single species, E. rangiferi, intro-
duced to northeastern North America through reindeer translocations
from Eurasia is restricted to Newfoundland (Lankester, 2001). Parelaphostrongylus andersoni

Parelaphostrongylus andersoni is a muscle-dwelling nematode of white-
tailed deer (O. virginianus) and caribou, with males measuring 19–23mm
and females around 30–35mm. It can cause significant muscular and pul-
monary disease in these hosts. Despite this pathogenicity and its broad
distribution, little is known about the ecology and impacts at the popula-
tion level in its main arctic host, the caribou.
Parasites in Ungulates of Arctic North America and Greenland     149

(a) Host and Geographic Distribution: White-tailed deer are considered

the primary hosts, with caribou colonized by host switching during the
Pleistocene (Carreno and Lankester, 1994; Asmundsson et al., 2008). Adult
nematodes were first found in caribou from central and eastern Canada,
including Newfoundland and it was presumed that DSL in caribou across
their range were P. andersoni (Lankester and Hauta, 1989; Lankester and
Fong, 1998; Ball et  al., 2001). Recent molecular identification of DSL in
several barren-ground and woodland caribou herds has confirmed the
­presence of P. andersoni and supports the hypotheses that this parasite
has a continuous distribution in barren-ground caribou across their arctic
range (Kutz et al., 2007). Despite sympatry of infected caribou herds with
various populations of muskoxen, moose and Dall’s sheep, P. andersoni
has not been detected in these other ungulate species (Jenkins et al., 2005a;
Kutz et al., 2007).
(b) Ecology: The life cycle of P. andersoni is typical of protostrongylids.
Parelaphostrongylus andersoni successfully developed to L3 in gastropod
intermediate hosts Triodopsis sp. and Mesodon sp. within 3–4 weeks under
laboratory conditions at 20–26°C (Pybus and Samuel, 1984a; Lankester
and Hauta, 1989) and was reported from wild Mesodon spp. and D. laeve
(Lankester and Fong, 1998; Anderson, 2000). In these studies, however,
larval identity was not confirmed using DNA-based techniques. Deroc-
eras laeve is considered one of the most important natural intermediate
hosts for P. andersoni in Newfoundland (Lankester and Fong, 1998) and is
found across most, if not all, the mainland North American caribou range
(Pilsbry, 1946; Kutz et  al., 2000b; Grimm et  al., 2009). Emergence of L3
from gastropods has not been investigated for P. andersoni. The prepatent
period in a single experimentally infected female caribou calf given 385
L3s was 66 days (Lankester and Hauta, 1989) and was within the range of
that reported for other cervid hosts (49–75 days) (Prestwood, 1972; Pybus
and Samuel, 1984b; Lankester et al., 1990). The migratory path of P. ander-
soni within the ungulate host has not been fully described.
The patent period for P. andersoni in experimentally infected caribou
and white-tailed deer appears to be quite short. In the only experimen-
tally infected caribou calf (given 295 L3 followed by 85 L3 14 days later),
Lankester and Hauta (1989) reported a low peak of 124 LPG of faeces two
weeks after patency (66dpi) followed by a significant drop to 7 LPG of
faeces by 32 days after patency. A similar pattern was observed in white-
tailed deer, with larval shedding peaking in 2–8 weeks post-patency
and then declining (Nettles and Prestwood, 1976; Pybus and Samuel,
1981). Higher larval output, longer peaks (12 weeks post-patency) and
longer periods of patency were observed in white-tailed deer fawns
experimentally infected with higher doses of L3 (1,000L3) (Pybus and
Samuel, 1984b). A short patency for P. andersoni in caribou was sup-
ported by data from naturally infected caribou in Newfoundland, where
150     Susan J. Kutz et al.

its co-occurrence with E. rangiferi and a putative cross-immunity seem

to decrease larval output of both elaphostrongylines. Also, in two cari-
bou herds in which P. andersoni occurred alone, larvae were found only
in small faecal pellets considered to be from calves and yearlings, and
larger pellets were DSL-negative (Ball et al., 2001). These data support
the fact that P. andersoni has a short patency period in caribou and is pri-
marily in young animals, although association of faecal pellet size with
caribou age should be interpreted cautiously. Notably, L1 of P. andersoni
have been confirmed based on molecular sequence data in adult barren-
ground caribou from several different herds (Kutz et al., 2007; G. Verocai,
S, Kutz, unpubl. obs.).
(c) Impacts: Adult nematodes, eggs and larvae of P. andersoni can cause
significant pathology in the skeletal muscles and lungs, respectively, and
clinical signs can be severe. Adult nematodes are found predominantly in
the skeletal muscles, typically in the longissimus dorsus and psoas, but
can also be found in other muscles and fat (Prestwood, 1972; Nettles and
Prestwood, 1976; Pybus and Samuel, 1981; Lankester and Fong, 1998).
Gross pulmonary lesions associated with the presence of eggs and L1
include petechial haemorrhages and whitish nodules and are similar to
those found in white-tailed deer (Lankester and Hauta, 1989; Lankester
and Fong, 1998). In naturally and experimentally infected caribou, lesions
associated with adult parasites include diffuse haemorrhage in the region
of the lower neck and back, tight muscles and fasciitis (Lankester and
Hauta, 1989).
In deer experimentally infected with a large number of L3 (5000), clini-
cal signs include included pain in the loin muscles, reluctance to stand,
weakness, marked discomfort in walking and falling to the ground fol-
lowing light pressure on the loin muscles (Nettles and Prestwood, 1976).
Based on clinical signs in experimentally infected deer, this degree of
pathology probably compromises the mobility in naturally infected
caribou. Moreover, co-infections with other common pulmonary nema-
todes such as Varestrongylus and Dictyocaulus might have an additive or
­synergistic effect leading to more severe verminous pneumonia. Parelaphostrongylus odocoilei

Parelaphostrongylus odocoilei is a muscle-dwelling protostrongylid common
in subspecies of O. hemionus (mule, Columbian black-tailed and Sitka black-
tailed deer) and Dall’s and Stone’s sheep and is occasionally reported from
mountain goats, bighorn sheep and woodland caribou (Table 2.5). The adult
nematodes have a size range from 24 to 33mm for males and 44 to 56mm
for females and typically occur in skeletal muscles, primarily of the back,
hind limbs, forelimbs and trunk but can be found elsewhere (Hobmaier
and Hobmaier, 1934; Pybus and Samuel, 1984b; Kutz et al., 2001d).
Parasites in Ungulates of Arctic North America and Greenland     151

(a) Host and Geographic Distributions: Parelaphostrongylus odocoilei was

described originally in mule deer and it occurs in this species through-
out western North America from California to southeastern AK (Hobma-
ier and Hobmaier, 1934; Brunetti, 1969; Platt and Samuel, 1978; Samuel
et  al., 1985; Lankester, 2001; Mortenson et  al., 2006). It is common and
widespread in thinhorn sheep south of the Arctic Circle with prevalence
approaching 100% in most infected populations (Jenkins et  al., 2005a).
It has not been found in Dall’s sheep from the Richardson Mountains
(YT, NT) or the Brooks Range (YT, AK) despite extensive faecal surveys
(Jenkins et  al., 2005a ; Jenkins et  al., 2007) (E. Hoberg, I. Asmundsson,
K. ­Beckmen unpubl. obs). It occurs in mountain goats in BC, NT and AK
(Jenkins et al., 2004). DSL are also reported from this host in AB and Wash-
ington State, USA, but have not been conclusively identified (Pybus and
Samuel, 1984a).
The distribution of P. odocoilei in caribou is less well understood and
there exist only two confirmed reports. A single DSL in a woodland caribou
from the Hay River region, NT, was identified as P. odocoilei by molecular
characterization (Jenkins et al., 2005a) and adult nematodes were recov-
ered from skeletal muscles of mule deer experimentally infected with DSL
from faeces of mountain woodland caribou from Jasper National Park,
AB (Gray and Samuel, 1986). These authors hypothesized that it could be
well established in other woodland caribou populations sympatric with
mule deer in AB and BC but to date this has not been confirmed despite a
moderate level of surveillance using DNA-based techniques (Kutz et al.,
2007; G. Verocai, S. Kutz unpubl. obs.).
Moose can be experimentally infected with P. odocoilei (Platt and Sam-
uel, 1978), but the parasite has not been found in faecal surveys of moose
sympatric with infected deer and/or thinhorn sheep in the YT, the Sahtu
Settlement Region NT, northeastern BC, or AK (Kutz et al., 2007). Parela-
phostrongylus odocoilei has not been reported in muskoxen, but nowhere is
this potential host sympatric with infected Dall’s sheep or mule deer.
(b) Ecology: The life cycle of P. odocoilei is similar to that of other tissue-
dwelling protostrongylids. Adults in the skeletal muscles are closely asso-
ciated with blood and possibly lymphatic systems, where females deposit
eggs that are carried to the lungs. A number of different arctic gastropod
species have been reported naturally or experimentally infected with lar-
vae of P. odocoilei, including D. laeve, Catinella spp. and Euconulus cf. fulvus,
but not members of the Pupillidae (Jenkins et al., 2006a) (Lankester, 2001).
As with many other protostrongylids of northern ungulates, D. laeve is
considered the most important intermediate host because of its abun-
dance, susceptibility and higher prevalence of infection in nature, when
compared to other gastropods (Samuel et  al., 1985). In the laboratory,
development in D. laeve occurs in as few as 10 days at approximately 24°C
152     Susan J. Kutz et al.

and L3 can develop within a single summer in experimentally infected D.

laeve in the Mackenzie Mountains, NT (Jenkins et al., 2006a).
Emergence of L3 from D. laeve occurs in the laboratory with approxi-
mately one-third of the total larvae emerging from days 22 to 60 post-infec-
tion at room temperature. Emerged L3 survive up to six months in darkness
in water at near-freezing temperatures. Emergence also occurs to a lesser
extent in Catinella sp. (Jenkins et al., 2006a). Emerged L3 might play an impor-
tant role in overwinter transmission when gastropods are not available, as
postulated for U. pallikuukensis (Kutz et al., 2000b; Jenkins et al., 2006a).
The prepatent period in three Stone’s sheep and two thinhorn hybrids
(O. d. stonei × O. d. dalli) each given 200 L3 from a Dall’s sheep source
ranged from 68 to 74 days (Jenkins et al., 2005b), up to 1–3 weeks longer
than that reported for mule and black-tailed deer infected with deer-source
P. odocoilei (Pybus and Samuel, 1984b). Larval shedding early in patency
was high, peaking at 14,000–30,000 LPG between 95 and 109dpi. Larval
counts remained high (1700–4800 LPG of dry faeces) and patency lasted
for a minimum of 180dpi at which point the animals were removed from
the study (Jenkins et al., 2005b).
In the Mackenzie Mountains, NT, larvae of P. odocoilei were present in
84–100% of Dall’s sheep faeces sampled from March 2000 to April 2003.
Intensity ranged from 141 to 1350 LPG through the year with larval pro-
duction peaking from March through May. There was no evidence of
age-related immunity (Jenkins et  al., 2006b). Experimentally infected
D. laeve maintained in natural conditions in the Mackenzie Mountains
yielded high numbers of L3 by August–September. It is hypothesized
that the majority of transmission might happen on the winter range,
with infection of gastropods once they emerge from hibernation in
spring and definitive host infection when the sheep return during fall
(Jenkins et al., 2006b).
The apparent absence of P. odocoilei in Dall’s sheep and other potential
host species from the Richardson Mountains and Brooks Range may result
from a combination of historical, climatic, physical and species barriers.
The parasite does not appear to have expanded from refugial habitats with
its hosts at the termination of the Pleistocene, a factor which may explain
current absence at high latitudes north of the Alaska Range (Schafer et al.,
2010; Hoberg et al., 2012). Outcomes using a degree–day model for devel-
opment in gastropod intermediate hosts suggest that temperature-related
constraints on development might limit establishment of P. odocoilei in
naïve Dall’s sheep populations at the northern extent of their range (Jen-
kins et al., 2006b). Under current climate warming scenarios, however, the
‘Arctic-adapted’ characteristics of P. odocoilei, including freeze tolerance of
free-living stages, high prevalence and larval production in Dall’s sheep,
larval emergence, high establishment and development rates in gastropod
Parasites in Ungulates of Arctic North America and Greenland     153

intermediate hosts, could allow it to persist if introduced into currently

non-endemic areas.
Introduction of P. odocoilei to the northern sheep ranges is unlikely to
be mediated through movement of sheep. Dall’s sheep are restricted to
mountain ranges and are not likely to disperse across vast expanses of tun-
dra or forest to colonize new mountain habitats, a hypothesis supported
by evidence of population fragmentation found in phylogeographic stud-
ies (Loehr et  al., 2006). Caribou in contrast are much more vagile and
conceivably could bridge the gap between mountain ranges during their
annual migrations and introduce the parasite to Dall’s sheep and muskox
populations further north. The potential suitability of caribou as mainte-
nance hosts for this parasite, however, remains enigmatic (see previous
discussion). Muskoxen conceivably could also serve a role in maintenance
and expansion of P. odocoilei between mountain ranges and Dall’s sheep
populations but susceptibility of this species is unknown. Considerably
more research is needed to understand the ecology and transmission
dynamics of P. odocoilei in this system and the potential for it to emerge
further north.
(c) Impacts: Parelaphostrongylus odocoilei is a significant pathogen in
Dall’s sheep, causing parasitic pneumonia and sporadic mortality events
in the wild (Jenkins et al., 2007), as well as weight loss, muscle atrophy
and neurological disease following experimental infection (Jenkins et al.,
2005b). The neurological symptoms developed two weeks before patency
and included ataxia of the hind legs, loss of conscious proprioception
and hyperaesthesia, all of which resolved at patency. Pybus and Samuel
(1984a,b) found adult nematodes and eggs in epidural fat of the spinal
cord in deer and Jenkins et  al. (2005b) detected eosinophilic pleocytosis
and antibody to Parelaphostrongylus spp. in the cerebrospinal fluid of the
experimentally infected animals, suggesting that this parasite migrates
through the central nervous system of thinhorn sheep. Haematogeneous
spread of eggs and larvae of P. odocoilei to the lungs during patency causes
significant pulmonary pathology manifested as a disseminated granulo-
matous pneumonia.
The neuromuscular pathology caused by P. odocoilei may enhance sus-
ceptibility to predation or accidents (e.g. falling off cliffs in the sheep’s
natural habitat) for animals with moderate to heavy natural infections
(Jenkins et  al., 2005b). Importantly, the parasite is quite small and dif-
ficult to detect, so mortality events associated with the adult stages may
be misdiagnosed as accidents or predation. Pulmonary failure due to P.
odocoilei was the cause of mortality in a 10-month-old, naturally infected
Dall’s lamb (S. Kutz, E. Jenkins, B. Elkin, A. Veitch unpubl. data) and
was a contributing factor in the deaths of other thinhorn sheep in the
wild (Jenkins et  al., 2007). In Dall’s sheep, P. odocoilei commonly co-
occurs with P. stilesi, a pulmonary protostrongylid (Jenkins et al., 2006a).
154     Susan J. Kutz et al.

These two species cause very different pulmonary pathology: P. odocoilei

diffuse granulomatous pneumonia and P. stilesi locally severe granulo-
matous pneumonia usually in the caudodorsal regions of the lungs. Co-
infections, therefore, might lead to additive pathology and more severe
disease. Emerging issues and knowledge gaps for the Protostrongylidae Potentially invasive protostrongylids

In addition to the protostrongylid fauna discussed above, there are a num-
ber of potentially invasive species at temperate latitudes. Shifts in climate
and landscape structure, changes in arctic ecosystems, translocations of
domestic species and translocations/reintroductions of, and invasions by,
free-ranging hosts, might facilitate northward range expansion of some of
these species (e.g. Kutz et al., 2009a,b; Hoberg, 2010). Among the species
of protostrongylids that are likely to invade and have significant conse-
quences are O. macrotis (Protostrongylinae); M. capillaris (Muelleriinae);
Varestrongylus alpenae (Varestrongylinae) and Parelaphostrongylus tenuis
and Elaphostrongylus rangiferi (Elaphostrongylinae).
Orthostrongylus macrotis is found in the trachea and bronchi of mule and
black-tailed deer and pronghorn (Antilocapra americana) in the western US
and southwestern Canada (Boddicker and Hugghins, 1969; Greiner et al.,
1974; Pybus, 1990; Belem et al., 1993). It is also reported rarely from moose
(Samuel et al., 1976) and elk (Honess and Winter, 1956). Northward range
expansion of mule deer may bring this parasite into sympatry with ungu-
lates in subarctic and arctic environments (deVos and McKinney, 2007;
Wilson, 2009). The literature on this lungworm is sparse and consequently
its ecology, pathology and impacts on hosts, as well as its potential for
invasion into northern ungulates, are unknown.
Muellerius capillaris is an important lung nematode of domestic sheep
and goats. It has spilled over to bighorn sheep in some regions of Canada
and the United States (Ezenwa et  al., 2010). It has not been reported in
free-ranging Dall’s sheep or muskoxen from North America but is found
in muskoxen in Norway (S. Kutz, B. Ytrehus, G. Verocai, unpubl. obs.).
Suitable gastropod species are present in the Arctic and Subarctic to sup-
port development of M. capillaris, and this parasite has a lower thresh-
old for development but it has a degree–day requirement similar to U.
pallikuukensis (Kutz et al., 2001c). It is likely, therefore, that if introduced,
environmental conditions and intermediate host diversity and abun-
dance would be suitable for establishment of M. capillaris. Ongoing and
new commercial or hobby farming activities of sheep adjacent to muskox,
Dall’s sheep or mountain goat range could lead to spill-over of this para-
site to free-ranging hosts.
Parasites in Ungulates of Arctic North America and Greenland     155

Varestrongylus alpenae. This is a pulmonary lungworm of white-tailed

deer in the eastern USA and southeastern and southcentral Canada, co-
occurring with P. tenuis and P. coburni (Dikmans, 1935b; Cheatum, 1951;
Gray et al., 1985). This species was linked to fatal pneumonia white-tailed
deer in northwestern USA (Cheatum, 1951). The susceptibility of arctic
ungulates to this parasite is not known; examination of woodland caribou
and moose in central and eastern Canada that are sympatric with infected
white-tailed deer may provide new insights.
Parelaphostrongylus tenuis. This is also a parasite of white-tailed deer
and causes severe neurologic disease in several other ungulate species,
including reindeer, caribou and moose (Lankester, 2001). This species is
widely distributed in white-tailed deer throughout eastern North Amer-
ica; in Canada, the western limit of its range is eastern Saskatchewan.
Parelaphostrongylus tenuis is considered a significant factor for failure of
caribou reintroductions in eastern Canada and Minnesota, USA, where
caribou were placed in areas sympatric with, or previously occupied by,
white-tailed deer (Trainer, 1973; Dauphiné Jr., 1975; Pitt and Jordan, 1994).
Climate and landscape changes are leading to a northward range
expansion of white-tailed deer and their parasites (Thompson et al., 1998;
Côté et al., 2004; Latham et al., 2011) but the potential for P. tenuis to sur-
vive and be transmitted at northern latitudes is currently unknown. This
will depend on both deer ecology and densities since white-tailed deer
are requisite for its maintenance (all other cervids are essentially dead-
end hosts or produce very few larvae that subsequent transmission is
unlikely), as well as the ability of larvae to develop and survive in subarc-
tic and arctic environments. Parelaphostrongylus tenuis is a risk to existing
woodland caribou and moose populations elsewhere in eastern Canada
(Lankester et al., 2007) and investigation of host–parasite dynamics at the
interface of these species may provide additional understanding of poten-
tial risks and implications for invasion of the Arctic.
Elaphostrongylus rangiferi. This is a common parasite of wild and semi-
domesticated reindeer (Rangifer tarandus tarandus) in Palaearctic regions
(Fennoscandia and Russia). It causes cerebrospinal elaphostrongylosis
(CSE) in Rangifer and experimentally infected moose (Lankester, 1977;
Lankester and Northcott, 1979; Stéen et  al., 1997; Lankester and Fong,
1998). It is a probable cause of a similar clinical disease in muskoxen in
Norway (Holt et al., 1990).
Elaphostrongylus rangiferi was introduced into Newfoundland with
infected reindeer from Norway in 1908 and is now well established in
woodland caribou across the island. Despite several opportunities for
translocation of E. rangiferi to North America with multiple other rein-
deer introductions (e.g. Lankester and Fong, 1989) the parasite has not
been detected in extensive faecal-based geographic surveys of caribou
and muskoxen on most of Canada’s mainland (Huby-Chilton et al., 2006;
156     Susan J. Kutz et al.

Kutz et al., 2007; G. Verocai, E. Hoberg, I. Asmundsson, S. Kutz unpubl.

obs.). Nor has it been detected in western AK, where the majority of the
introduced reindeer from Russia and Norway were established and are
now maintained as a commercial livestock activity (Oleson, 2005; Finstad
et al., 2006). Clinical disease has not been detected in the semi-domesti-
cated reindeer or adjacent free-ranging caribou herds; however, clinically
affected animals may quickly succumb to predation and with abundant
scavengers and a rare human presence carcasses are unlike to be detected.
Even the semi-domesticated reindeer are free ranging over a wide geo-
graphic, sparsely populated area and are rarely observed except during
brief annual handlings for deworming. There have also not been any spe-
cific survey with subsequent larval identification for protostrongylids in
this area, so the presence of E. rangiferi associated with reindeer herds in
AK cannot be ruled out.
The possibility remains that E. rangifer has established elsewhere in
North America but remains undetected. Deroceras laeve is a suitable inter-
mediate host (reviewed in Lankester, 2001) and is common and wide-
spread across most of mainland arctic and subarctic Canada (Pilsbry,
1946). The L1 are freeze tolerant, and no clear decrease in larval survival
was observed in larvae held at −20°C (Lorentzen and Halvorsen, 1986).
Preventing its establishment in arctic North America, however, may be a
relatively high threshold temperature as well as a high number of degree
days required for development compared to other arctic protostrongylids
(Halvorsen and Skorping, 1982; Kutz et al., 2001c).
In order for invasive protostrongylids to successfully establish at sub-
arctic and arctic latitudes, suitable climatic conditions and adequate num-
bers and density of suitable intermediate and definitive hosts are critical,
as is a sufficient founding parasite population. These requirements will
differ among species, but some of the parasite characteristics that might be
important for establishment include freeze tolerance of immature stages,
overwintering ability (transposition of the barrier posed by harsh winter
conditions), broad host range, high larval production, and long lifespans.
This is applicable to other species in other nematode families and virtually
any other metazoan parasite. Advances in the identification of parasites and infected hosts

Biodiversity survey and inventory have resulted in significant advances
in a knowledge of the distribution of Protostrongylidae species infect-
ing ungulates in high latitudes of North America (Hoberg et  al., 1995;
Kutz et  al., 2001b; Jenkins et  al., 2005a; Kutz et  al., 2007; Hoberg et  al.,
2008b). Less than two decades after the recognition of a new genus of
protostrongylid in muskoxen from the Central Canadian Arctic (Hoberg
et  al., 1995), the definition of new host and geographic ranges for two
other protostrongylids and discovery of yet another previously unknown
Parasites in Ungulates of Arctic North America and Greenland     157

species that is widespread through northern North America (Kutz et al.,

2001d; Hoberg et al., 2002; Kutz et al., 2007) show us that there remains
much to be revealed. Recent and substantial advances in the knowledge
of protostrongylid faunas are partially due to the development and use of
molecular techniques that permit species identity based on single L1s in
faeces. These methods supplant laborious bioassay trials and equivocal
assessments of larval morphology, which were impediments to definitive
identification of parasites and infected hosts (Jenkins et al., 2005a; Huby-
Chilton et  al., 2006; Kutz et  al., 2007). Importantly, previous records of
protostrongylids not validated with either adult specimens or sequencing
of larval DNA remain suspect. Application of molecular-based diagnos-
tics has already facilitated large-scale studies, both geographically exten-
sive and site intensive, on parasite biodiversity which have eliminated
the need for necropsy and examination of adult nematodes (Jenkins et al.,
2005a; Kutz et al., 2007; Asmundsson et al., 2008). The development and
application of new and affordable molecular diagnostics approaches that
permit rapid identification of high numbers of protostrongylid larvae has
immediate value for screening ungulate populations prior to management
and conservation activities such as translocations. Ecology
In general, protostrongylid species appear highly adapted to inhospitable arc-
tic environmental conditions. Arctic adaptations include a series of ecologi-
cal traits such as cold and freeze tolerance in both L1 and L3, emergence of L3
from the gastropod host, extended patency (e.g. U. pallikuukensis, P. odocoilei)
and cumulative infections in some species of long-lived hosts. Not all arctic
protostrongylids display all of these traits but they persist nonetheless. For
example, despite a relatively short period of patency and low larval produc-
tion, P. andersoni has a vast geographic range across the mainland Arctic and
Subarctic. Its distribution mirrors that of its only known arctic host, the cari-
bou. Strategies used by this parasite that allow it to persist across such a large
area in a single host species, when the closely related elaphostrongyline,
P. odocoilei, cannot, may be linked to a combination of historical host–parasite
associations and colonization events as well as tolerance and resilience to
contemporary ecological conditions (e.g. Hoberg et al., 2012c).
The protostrongylid species in arctic ungulates appear to have varying
degrees of host specificity, ranging from apparently absolute with U. pal-
likuukensis, parasitic only in muskoxen, to generalists such as P. odocoilei
which is found naturally infecting caribou, Dall’s sheep and mountain goats
and experimentally can infect moose. In some cases when obvious ecologi-
cal barriers have been removed, such as when muskoxen were introduced
or expanded onto Dall’s sheep range, parasites have successfully colonized
new hosts (e.g. P. stilesi in muskoxen, although persistence in muskoxen
in the absence of sheep has not been demonstrated). In other cases where
158     Susan J. Kutz et al.

there are no obvious ecological barriers, parasites retain apparent host

specificity. For example, despite caribou being sympatric with Dall’s sheep
and muskoxen across large parts of their range, P. andersoni has not been
detected in these latter two species (see also Asmundsson et al., 2008). Some
of these species cross taxonomic boundaries of hosts, infecting both cervids
and bovids (e.g. P. odocoilei, Varestrongylus) while others remain within sub-
family or family boundaries (e.g. Protostrongylus in Caprinae, P. andersoni
in cervids). In the case of moose, this species appears to be an accidental
host, only naturally and rarely infected with Varestrongylus sp. n. in the Arc-
tic. Understanding how this mosaic of protostrongylids circulates among
arctic ungulates requires an integrative approach examining deep histori-
cal events of host and parasite colonization of North America, population
genetics and phylogenetic and phylogeographic studies of the parasites
and contemporary ecological studies (e.g. Hoberg et al., 2012b).
A major and essential component of the protostrongylid life cycle that
remains poorly defined for the Arctic is the ecology of the gastropod inter-
mediate hosts. The literature on arctic gastropods is sparse and limited to
a few species distributions (Pilsbry, 1946; Kutz et al., 2000b; Grimm et al.,
2009). This aspect of the life cycle has the potential to be very dynamic and
responsive to climate, with changing temperature and hydrological condi-
tions in the Arctic likely to have substantial impacts on the biodiversity
and population dynamics of gastropods. The role of aquatic gastropods
as intermediate hosts deserves further investigation. These intermediate
hosts may become increasingly important under climate change scenarios
where a warmer environment together with increased precipitation and
flooding events may favour parasite species capable of infecting aquatic
gastropods (reviewed in Morley, 2010). Intricately linked to studies on gas-
tropods are those on host movement, habitat use and grazing behaviour.
Such knowledge provides information on environmental contamination
and sources and rates of exposure. Understanding this complexity may
help tease out some of the ecological features which determine apparent
host and geographic distributions.
Climate change is a major feature of arctic landscapes and protostron-
gylids are repeatedly demonstrated as being highly responsive to climate
warming (Handeland and Slettbakk, 1994; Ball et al., 2001; Jenkins et al.,
2006b). Current climate warming conditions are likely to decrease devel-
opment times and increase survival rates for protostrongylids endemic
to ungulates in the North, extend the period of the year when parasite
transmission is possible and lead to expansion of geographic ranges of
endemic and invasive protostrongylids (Kutz et  al., 2005; Hoberg et  al.,
2008a, 2008b; Kutz et al., 2009b). Disease outbreaks may be triggered by
unusually warm summers such as has occurred in reindeer in northern
Europe infected with E. rangiferi (Handeland and Slettbakk, 1994) or by
Parasites in Ungulates of Arctic North America and Greenland     159

invasions of new protostrongylids into naïve host populations (Ball et al.,

Mechanistic models have been developed and validated for predicting
the development and response to climate of two key arctic protostrongylids
(U. pallikuukensis and P. odocoilei) in gastropods on the tundra. These have
served as useful tools for examining the past, current and future distribu-
tion of these parasites and can provide an insight into the ecology of other
protostrongylids if basic life cycle information (development thresholds
and heating constants) is available. These models require further develop-
ment to move into a more quantitative predictive realm that will allow
identification of the key stages of the life cycle that are sensitive to change. General effects

Protostrongylids can cause significant multi-systemic pathology. Exacer-
bating the effects on the individual is the fact that caribou, muskoxen,
Dall’s sheep and mountain goats are each susceptible to at least three
separate species of protostrongylids, and co-infections with at least two
species are confirmed in all hosts. While the basic pathology has been
described for most (but not all) northern protostrongylids, the potential
additive effects of co-infections require further investigation. Similarly,
while there is a small literature that demonstrates potentially subtle pop-
ulation-level effects of protostrongylids in bighorn sheep and snowshoe
hares (Festa-Bianchet, 1991; Murray et  al., 1997), the role of protostron-
gylids in the population dynamics of arctic ungulates in North America
is yet to be examined. Subfamily Dictyocaulinae Dictyocaulus spp.

Dictyocaulus spp. are large (up to several centimetres long) white nema-
todes found typically with a dorsal distribution in the bronchi and bron-
chioles of the lungs. A number of species are found in a broad range of
free-ranging ungulate hosts across the Holarctic (Hoglund et  al., 2003).
There are varying degrees of host specificity.
(a) Host and Geographic Distributions: At least one species – Dictyocaulus
eckerti – is recorded in moose and caribou in AK, and muskoxen from the
Kitikmeot region of NU and northern QC. Dictyocaulus viviparus has been
reported from muskoxen on the arctic islands and mainland NT and NU,
Canada, as well as AK but these records should be considered suspect
(Table 2.5) (Gibbs and Tener, 1958; Samuel and Gray, 1974; USNPC, 2011).
Records of D. viviparus have often been based uncritically on adult and/or
larval morphology and in light of recent genetic and morphological work
it is more likely that these are D. eckerti (Divina et al., 2000; Hoglund et al.,
160     Susan J. Kutz et al.

2003). There are no published reports for Dictyocaulus in Dall’s sheep or

mountain goats but D. filaria has been reported in bighorn sheep from the
USA (USNPC, 2011). In Greenland, Dictyocaulus sp. was observed in one
of five caribou calves of the Akia-Maniitsoq herd examined in April 2008
(C. Cuyler, S. Kutz, unpubl. data).
(b) Ecology: Adult nematodes produce eggs that pass up the trachea
and, depending on the species, larvated eggs or larvae are excreted in the
faeces. The life cycle is direct and infection is by ingestion of infective L3.
The development from eggs or L1 in the environment is temperature and
humidity dependent. Data on larval development in the environment are
not available for D. eckerti, but for D. filaria of domestic sheep, develop-
ment of L1 to infective L3 in northeast England took approximately 4–9
days in spring and summer, 1.5–4 weeks in autumn and 5.5–7 weeks in
winter (Gallie and Nunns, 1976). The persistence of Dictyocaulus in musk-
oxen as far north as Bathurst Island at 75° latitude (Samuel and Gray, 1974)
suggests that it can develop to infective L3 in the short high arctic summer.
Extended survival of L3 in the arctic environment is unlikely. Whether dis-
persal of the infective larvae of Dictyocaulus spp. in the Arctic is facilitated
by spores of the faecal fungus Pilobolus released from the sporangia, as
occurs for at least some species (e.g. D. viviparus in cattle) (Eysker, 1991),
is not known.
Inhibited development is an important phenomenon in the life cycle
of D. filaria, with a large proportion of the eggs and larvae ingested in
the autumn inhibiting until the following spring (Ayalew et al., 1974). A
similar pattern of inhibition is expected for Dictyocaulus in muskoxen.
In commercial muskox harvests on Banks Island, NT, adult nematodes
are most common in yearling animals in early winter (typically Novem-
ber) and are rare or absent in February (M. Branigan, pers. comm), sug-
gesting that Dictyocaulus at this latitude may overwinter as inhibited
(c) Impacts: In general for Dictyocaulus spp., developing pre-adult lar-
vae, adults, eggs and hatched larvae can cause significant pulmonary dam-
age and respiratory disease in their hosts. In muskoxen on Banks Island,
NT, Dictyocaulus infections were associated with emaciation and mortal-
ity in yearlings on at least one occasion (Gunn et al., 1991b). Dictyocaulus
eckerti can also cause significant disease in reindeer and histopathological
findings in this host are consistent with those described in domestic live-
stock (Rahko et al., 1992).
The biodiversity of Dictyocaulus circulating in ungulates at high lati-
tudes remains poorly defined. There exist only a few patchy reports where
species identifications have been confirmed in North America. Where this
has occurred, the species has been designated as D. eckerti, refuting previ-
ous records of D. viviparus. Anecdotal evidence suggests that Dictyocaulus
may be a significant cause of morbidity and mortality of young muskoxen
Parasites in Ungulates of Arctic North America and Greenland     161

FIGURE 2.8  Tissue and lymphatic Spirurida reported from ungulates of arctic North
America, including Greenland.

and perhaps also caribou. That it persists in the harsh high Arctic environ-
ment in low-density host populations is perhaps surprising and further
exploration of the ecology of the free-living and parasitic stages of this
parasite is warranted.

2.3.3. Other tissue nematodes: Onchocercidae

There is a minimum of three genera of Onchocercidae nematodes circulat-
ing in ungulates of arctic Canada and AK; none have been reported from
Greenland (although see Fielden, 1877) (Fig. 2.8). Depending on genus
and species, adult nematodes may be found in the abdominal cavity, con-
nective tissue or lymphatic system of their hosts, whereas larval forms
are found in the blood or lymph. These larval forms, named microfilariae
(L1), are typically transmitted by haematophagous dipteran insect inter-
mediate hosts in which development to infective L3 occurs. Subfamily: Setariinae Setaria spp.

Setaria spp. are robust nematodes 10–90mm long and 1–3mm thick found
in the peritoneal cavity of a variety of ungulates (Becklund and Walker,
1969; Laaksonen et al., 2007). Two species have been identified in North
American wild ungulates: S. yehi and S. labiatopapillosa. Setaria yehi is con-
sidered distinct from S. tundra, the main species parasitizing cervids in
Fennoscandia (Becklund and Walker, 1969). According to Nikander et al.
(2007), however, the morphological differences between these nominal
species are less than the intraspecific variation demonstrated within S.
tundra. The potential synonymy for S. yehi and S. tundra requires further
exploration; the occurrence of a single holarctic species may be consistent
with the recent history for moose or caribou at high latitudes (Rehbinder
162     Susan J. Kutz et al.

et  al., 1975; Laaksonen et  al., 2007; Nikander et  al., 2007; Hoberg et  al.,
(a) Host and Geographic Distributions. Setaria yehi is found in cervids
across a broad geographic range, documented in reindeer, caribou and
moose from AK and caribou in the NT (Table 2.5) (Becklund and Walker,
1969; Dieterich and Luick, 1971; A. Quist, K. Beckmen unpubl. obs.). Setaria
labiatopapillosa is typically a parasite of bovids but has been reported from
caribou and moose at temperate latitudes (Becklund and Walker, 1969;
USNPC, 2011); at least some of the records from moose may actually be of
S. yehi. There are no reports of Setaria in muskoxen, Dall’s sheep or moun-
tain goats but S. labiatopapillosa has been reported from bighorn sheep
(Becklund and Walker, 1969), indicating that North American caprines
may harbour Setaria species. Setaria sp. are also common in wood bison in
the NT (B. Elkin, unpubl. obs.).
(b) Ecology: The ecology of S. yehi in the Arctic has not been investigated.
A series of studies on S. tundra, however, provide valuable insight into
the ecology of these species in ungulates at arctic and subarctic latitudes.
Adult nematodes live in the peritoneal cavity and produce microfilariae
that circulate in the blood stream (Laaksonen et al., 2009b). Haematopha-
gous insects including mosquitoes (Culicidae, especially Aedes spp. for S.
tundra) and horn flies (Haematobia spp.) are intermediate hosts (Laaksonen
et  al., 2009a). Development of microfilariae to L3 in the insect is tem-
perature dependent and for S. tundra takes 14 days at 21°C but does not
occur at a mean temperature of 14.1°C (Laaksonen et al., 2009a). Animals
are exposed to S. tundra during the summer and the prepatent period in
reindeer is approximately four months, with microfilaria first detected in
calves in early November. Thus, in arctic environments, animals infected
one summer will not contribute to transmission until the following year.
Patterns of microfilariae in the peripheral blood vary with age, sea-
son and activity levels. Prevalence and density of microfilariae tend to
be higher in calves than in adults for S. tundra in reindeer and moose
(Laaksonen et al., 2007; Laaksonen et al., 2009b) and similar results were
reported for Setaria sp. in black- and white-tailed deer from southern lati-
tudes of North America (Weinmann et al., 1973; Prestwood and Nettles,
1977). Density of microfilaria in the peripheral blood is the highest dur-
ing the summer. Microfilarial density also increases with host activity and
may enhance transmission during periods of insect harassment, when
hosts are more active due to the discomfort caused by bites and presence
of insects (Laaksonen et al., 2009b). In six captive reindeer, microfilariae-
mia peaked from June to mid-September, then decreased and disappeared
by January (n = 3) or remained very low until the following summer (n = 3),
suggesting a one-year lifespan for the adult parasite and/or evidence of
acquired immunity. Patterns of disease outbreaks in reindeer in Finland –
emerging initially in the south and then moving to the north while disease
Parasites in Ungulates of Arctic North America and Greenland     163

in the south decreased – also support an acquired immunity in reindeer.

There is no evidence for transplacental ­transmission in reindeer.
Moose sympatric with infected reindeer populations have a very low
prevalence of S. tundra (1.4–1.8%) suggesting that they are not good hosts
for this parasite (Laaksonen et al., 2007; Laaksonen et al., 2009b). However,
in some regions of AK, S. yehi appears to be well established in moose with
prevalence of microfilariae up to 100% (A. Quist, K. Beckmen unpubl.
Setaria is highly sensitive to climatic conditions and disease outbreaks
and range expansions of S. tundra in Fennoscandia are linked to unusu-
ally warm climatic conditions. In Finland, disease outbreaks in reindeer
have occurred following two consecutive summers with warmer than
average temperatures. Models developed to describe these outbreaks
suggest that disease emergence results from increased development
rates and abundance of the parasites in vectors as well as the herding
behaviour and habitat use of the reindeer (Laaksonen et al., 2009a; Laak-
sonen et al., 2010a).
(c) Impacts: Unlike the situation in Fennoscandia with S. tundra, S.
yehi does not currently seem to be an important cause of morbidity
and mortality in wild caribou of North America. Clinical disease is not
reported in caribou and it was not found in post-mortem examinations
of several hundred wild caribou during International Polar Year activi-
ties (S. Kutz and CARMA, 2011). In AK, infections of 5–20 adult S. yehi
in captive adult reindeer caused a mild to moderate peritonitis but no
clinical signs (Dieterich and Luick, 1971). In contrast, and much more
recently, intense inflammation, a secondary bacterial peritonitis and
mortality in nine free-ranging moose calves were attributed to migrat-
ing S. yehi and massive numbers of microfilaria (A. Quist, K. Beckmen
unpubl. obs.). Subfamily Onchocercinae Onchocerca spp.

In North America, Onchocerca cervipedis (syn. Wehrdikmansia cervipedis),
commonly known as ‘legworm’ or ‘footworm’, is a common parasite of
cervids, including moose and woodland caribou of the boreal regions of
AB, BC and southern AK (Ritcey and Edwards, 1958; Williams and Babero,
1958; Low, 1976; Samuel et al., 1976). Adult nematodes range from 5.5 to
6cm (males) and 1.8 to 2.0cm (females) and are found in nodules within
subcutaneous tissues (Wehr and Dikmans, 1935). Parasite identification
is based mainly on gross morphology and the presence of subcutaneous
nodules containing intra-lesional adult nematodes and/or microfilariae
(Samuel et  al., 1976). In Eurasia, Onchocerca skrjabini (Synonym O. tarsi-
164     Susan J. Kutz et al.

cola), is present in reindeer and moose (Bylund et al., 1981). Nodules in

reindeer are mainly present under the skin of the muzzle, hocks and to
a lesser extent elsewhere on the body including the brisket and shoulder
(Lisitzin, 1964).
(a) Host and Geographic Distributions. Until recently, there were only
anecdotal reports of O. cervipedis in moose from AK and the YT (Table 2.5)
(P. Merchant, pers. comm.) Recent findings, based on combined parasite
identification, including molecular and histopathological methods, have
confirmed that O. cervipedis occurs in moose and Grant’s caribou from
AK and moose from the NT (G. Verocai, K. Beckmen, S. Kutz, E. Hoberg
unpubl. obs.). The occurrence of this parasite in muskoxen, Dall’s sheep
and mountain goats is unknown. Onchocerca cervipedis may be much more
widespread in ungulates of arctic North America, however, and the need
for targeted survey is apparent.
(b) Life Cycle: The microfilariae produced by female parasites remain in
the skin and are ingested by the vectors during feeding. Blackflies (Dip-
tera: Simuliidae) act as intermediate hosts, with microfilariae developing
to L3. Pledger (1978) demonstrated that Simulium decorum and Simulium
venustum serve as intermediate hosts of O. cervipedis in northeastern AB,
although other simuliids were found feeding on moose. Intermediate
hosts species involved in the epidemiology of this parasite in high lati-
tudes of North America are not known but species that serve as interme-
diate hosts in AB, and related species, are widely distributed in AK, YT,
NT and NU (Currie, 1997; Currie and Adler, 2000; Currie, 2006; Adler and
Currie, 2008).
(c) Impacts: Oncocherca cervipedis rarely causes significant clinical signs.
There are occasional reports of massive infections resulting in swelling,
ulceration and hoof damage in Odocoileus spp. (Rush, 1935; Herman and
Bischoff, 1946). De Nio and West (1942) postulated that clinically affected
animals would be more susceptible to predation and an easier target to
hunters. In contrast, in moose and caribou, this parasite is generally found
along the metatarsus and metacarpus (DeNio and West, 1942). Clinical
disease has not been described in caribou but infections in moose from
YT were associated with open sores in the lower legs (P. Merchant, pers.
comm.). The impacts of O. cervipedis on cervid populations in high lati-
tudes of North America are unknown. Some species of Onchocerca can be
zoonotic, and a recent study reported that Onchocerca jakutensis, a species
that normally infects wild cervids from Eurasia, causes nodular dermato-
logical disease in people (Koehsler et al., 2007).
Parasites in Ungulates of Arctic North America and Greenland     165 Subfamily: Splendidofilariinae Rumenfilaria andersoni

Rumenfilaria are nematodes located in the subserosal lymphatic vessels or
veins of the rumen. Males are up to 62mm long and females up to 205mm
long and may be visible to the naked eye in older and/or thin animals
(Lankester and Snider, 1982; Laaksonen et al., 2010b).
(a) Host and Geographic Distributions: Rumenfilaria andersoni was first
described in moose from northwestern Ontario in 1982 (Lankester and
Snider, 1982) and until recently was only known from the original descrip-
tion. Surveys have now detected microfilariae consistent with R. andersoni
in the blood of up to 70% of Alaskan moose (A. Quist, K. Beckmen unpubl.
obs.). Rumenfilaria has not been documented in muskoxen, Dall’s sheep,
mountain goats or caribou from North America. Rumenfilaria andersoni
tends to be common in other regions where there has been targeted sur-
vey, for example, in Finland (Laaksonen et al., 2010b), and the absence of
reports in caribou, and perhaps other ungulates, in arctic North America
may reflect a lack of search effort as opposed to true absence. Conspeci-
ficity of populations in Fennoscandia and North America remains to be
Life Cycle: Microfilariae are easily detected in the blood of infected ani-
mals (Laaksonen et al., 2010b), and based on what is known for related
genera it is probable that transmission is by haematophagous arthropods.
Impacts: Adults obstruct the lymphatic vessels of the rumen leading
to dilatation, lymphaedema, lymphangitis, granulomatous inflammation
and fibrosis (Laaksonen et al., 2010b). The occurrence of clinical disease in
wild ungulates remains unknown. Emerging issues and knowledge gaps for the Onchocercidae

Until recently, the Onchocercidae were a completely neglected compo-
nent of the helminth fauna of arctic ungulates of North America. Recent
mortality events for moose calves in AK, new observations of Onchocerca
in moose and caribou in northern Canada and major mortality events in
Fennoscandia linked to S. tundra highlight the possibility that these could
become, or may be becoming, important emerging pathogens under cur-
rent scenarios for climate change. In particular, the work in Fennoscandia
has demonstrated that these parasites are highly responsive to climatic
conditions and that small changes in summer temperatures can lead to
significant disease outbreaks. Members of the Onchocercidae are also
important pathogens of humans in the tropics and knowledge gained from
studying their ecology in the Arctic may provide insights into manage-
ment of this group of parasites in other regions (Laaksonen et al., 2010a;
Davidson et al., 2011). Further research on the biodiversity, definitive host
166     Susan J. Kutz et al.

FIGURE 2.9  Cestoda reported from ungulates of arctic North America, including Greenland.

TABLE 2.6  Cestodes reported from ungulates of arctic North America, including
Greenland. The range of prevalence reported is indicated below the parasite name. Only
prevalence estimates based on sufficient sample sizes are included. Data compiled from
available published and grey literature

Host, Parasite Herd, region or nearest place name

Echinococcus granulosus AK Not specifieda; Teshekpuk, Northern Alaska
(1.3-20%) Peninsula, Mulchtna, Western Arcticb
NT Mackenzie Deltac–e; Beverlyf
QC/NL Rivière Georgeg
Taenia hydatigena (15- AK Teshekpukb; Not specifieda,c,h
60%) NT Mackenzie Deltac,e; Beverlyf
NU Kitimeot Regioni
QC Rivière-aux-Feuillesj
Taenia krabbei AK Northwest, Southcentral, Interiork
Taenia cf. krabbei AK Teshekpuk, Northern Alaska Peninsula, Mul-
(13–20%) chatnab, Not specifieda,h
NT Mackenzie Deltae,w
NU Kitikmeot Regioni
QC Rivière-aux-Feuillesj
GL Kangerlussuaql
Moniezia cf. expansa GL Kangerlussuaql
Avitellina arctica NT/NU Thelon Game Sanctuarym
QC Rivière Georgen
Dall’s sheep
Taenia hydatigena (35%) AK Not specifiedh
NT Mackenzie Mountainso
Moniezia sp. (10–16%) NT Mackenzie Mountainso
Parasites in Ungulates of Arctic North America and Greenland     167

TABLE 2.6  (continued)

Host, Parasite Herd, region or nearest place name

Echinoccocus granulosus AK South Centralp; Tanana Flats, Fairbanks, Palmerb
(24%) NT Mackenzie Mountainsq
Taenia arctos AK Interior and South Centralk
Taenia krabbei AK Interiork
Taenia cf. krabbei AK Not specifiedh
NT Mackenzie Mountainsq
Echinoccocus granulosus NT/NU Thelon Game Sanctuaryr
Taenia cf. hydatigena AK Not specifiedh
NT/NU Not specifiedq; Thelon Game Sanctuaryr
GL Hurry Inlets
Taenia cf. krabbei AK Not specifiedh
GL Kangerlussuaqt
Taenia sp. NU Ellesmere Islandu
GL east Greenlandv
Anoplocephalidae egg NU Bathurst Island and Devon Islandu,w
Moniezia expansa NU Ellesmere Islandq; Thelon Game Sanctuaryr
Moniezia sp. AK Nunivak Islandw
NU Ellesmere Islandx
a  Hadwen (1922). m  Gibbs (1960).
b  K. Beckmen (unpubl. data). n  USNPC, (2011).
c  Broughton et al. (1967). o  Simmons et al., (2001).

d  Sweatman and Williams (1963). p  Rausch (1959).

e  Choquette et al. (1957). q  S. Kutz, C. Tobac (unpubl. obs.).

f  Thomas (1996). r  Gibbs and Tener (1958).

g  Parker (1981). s  Alendal and Helle (1983).

h  Dieterich (1981). t  Raundrup et al. (2012).

i  Gunn et al. (1991a). u  Webster and Rowell (1980).

j  Ducrocq and Lair (2007). v  Fielden (1877).

k  Lavikainen et al. (2011). w  Samuel and Gray (1974).

l  Clausen et al. (1980). x  Tener (1954).

and geographic range of Onchocercidae in arctic ungulates, together with

research on the life cycle, intermediate host species, transmission patterns
and response to climate change are required (Fig. 2.8).
168     Susan J. Kutz et al.


The cestodes present in arctic ungulates are from two families, the Tae-
niidae, for which ungulates are intermediate hosts, and the Anoploce-
phalidae, for which ungulates are definitive hosts. Members of Taeniidae
include species of Taenia and Echinococcus, whereas the Anoplocephalidae
is represented by Moniezia, Avitellina and perhaps Thysanosoma (Figure 2.9,
Table 2.6).

2.4.1. Ungulates as Intermediate hosts: Taeniidae Subfamily Taeniinae Taenia hydatigena, Taenia krabbei and Taenia arctos
(a) Host and Geographic Distributions. The three species of Taenia recognized
at high latitudes in North America, T. hydatigena, T. krabbei and Taenia arc-
tos all have apparently Holarctic distributions in arctic ungulates, canids
and ursids (Table 2.6) (Loos-Frank, 2000; Haukisalmi et al., 2011). Larvae
are simple cysticeri that commonly occur in the liver and omentum, or
elsewhere in the peritoneal cavity (T. hydatigena) or in the heart, tongue,
oesophagus and skeletal musculature, and less commonly the brain
(T. krabbei and T. arctos) (Broughton et  al., 1967; Choquette et  al., 1957;
Gibbs and Eaton, 1983; Lavikainen et al., 2011).
Taenia krabbei is often listed as a subspecies of T. ovis, a designation now
refuted by molecular evidence (Lavikainen et al., 2010). A recent report of T.
ovis krabbei in a muskox from west Greenland (Raundrup et al., 2012) should
be referred to T. cf. krabbei; however, it is also possible that this represents T.
arctos instead (see Haukisalmi et al., 2011). Taenia arctos is morphologically
similar to, but genetically distinct from, T. krabbei. It was recently described
to be circulating in moose from AK and Finland and brown bears (Ursus
arctos) in Finland (REFS) (Haukisalmi et al., 2011; Lavikainen et al., 2011).
Consequently, all previous species-level identifications of T. krabbei require
re-evaluation by both morphological and molecular criteria to establish
identity. In particular, current records of T. krabbei in non-canid hosts may
not represent this species (e.g. Rausch, 1994; Hoberg et al., in press-a). Taenia
arctos and T. krabbei are considered phylogenetically quite distant, with the
former as a putative sister species to T. solium and T. krabbei as a sister to T.
multiceps. Since both species had been reported to infect moose, previous
records of T. krabbei in these intermediate hosts should be revisited (Lavi-
kainen et al., 2011). We refer historical records of T. krabbei as tentative and
use the designation of T. cf. krabbei in further discussions below. We treat T.
hydatigena similarly, since limited morphological and molecular confirma-
tion of species identity in arctic ungulates has been done.
Parasites in Ungulates of Arctic North America and Greenland     169

Taenia cf. hydatigena is reported in caribou, muskoxen, moose and Dall’s

sheep across their arctic ranges (Table 2.6) (Gibbs and Tener, 1958; Tener,
1965; Webster and Rowell, 1980). Taenia cf. krabbei is known in caribou,
moose and muskoxen but has not been reported in Dall’s sheep. Taenia
arctos was recently described to be circulating in moose and brown bears
(Ursus arctos) from AK and Finland (Haukisalmi et al., 2011; Lavikainen
et al., 2011). Taenia parenchymatosa, a taeniid typical in Eurasian reindeer,
was reported in the liver of reindeer from Alaska (Pushmenkov, 1945 cited
in Choquette et  al., 1957) and was probably introduced with these cer-
vids from Chukotka in the last century. It is unknown as to what extent
this parasite established in North America. Infections may be pathogenic
as indicated experimentally where one reindeer died following rupture
of the liver (Pushmenkov 1945 cited in Choquette et al., 1957; Jones and
Pybus, 2001).
(b) Ecology: Taenia spp. have a predator–prey life cycle with adult ces-
todes occurring in the small intestines of carnivores or omnivores and lar-
val stages found as cysts in tissues of herbivore hosts (Loos-Frank, 2000;
Jones and Pybus, 2001). Infection of the definitive hosts is by ingestion of
protoscolices from cysticerci in infected ungulates, and intermediate hosts
are infected by ingestion of eggs from the faeces of carnivores. Transpla-
cental transmission of T. cf. hydatigena was observed in a wild muskox
foetus on the mainland of western Nunavut, Canada (S. Kutz, J. Nishi
unpubl. data). Taeniid eggs are robust, can survive for extended periods
(>200 days) at cool temperatures (Gemmel, 1977) and are likely to per-
sist for extended periods in the Arctic. Infection prevalence and intensity
increases with age for T. cf. hydatigena in moose and caribou (­Addison
et  al., 1979; Thomas, 1996, although see Pollock et  al., 2009) and for
T. cf. krabbei (possibly T. arctos) in moose (Addison et al., 1979). Viable and
degenerate cysts are found across a wide age range of animals, suggesting
both a finite lifespan for the cysticerci as well as ongoing infection (Addi-
son et al. 1979). In caribou, prevalence of T. cf. hydatigena tends to decrease
from December to March (Thomas, 1996).
A series of experiments on T. cf. krabbei and T. hydatigena by Sweatman
and Henshall (1962) provide some important insights into characteristics
of the lifecycles of Taenia spp. in the context of arctic systems. For T. cf.
krabbei, the prepatent period in two dogs given cysticerci that originated
from reindeer from northern Canada was 34 and 37 days. This is short
compared to that for T. ovis in the same study (~60 days) (Sweatman and
Henshall, 1962). The prepatent period of Echinococcus multilocularis is
similarly short (Rausch and Schiller, 1956) and Sweatman and Henshall
(1962) suggested that both these species appeared to have evolved at high
latitudes and that the short prepatent periods could be adaptations to the
short arctic summers, allowing carnivores to maximize egg production
during the seasonal period when successful transmission to the interme-
170     Susan J. Kutz et al.

diate host is more likely. These species have extended histories at high lati-
tudes (e.g. Hoberg et al., 2012 ) and have been influenced by increasingly
cold environments since the Pliocene.
Establishment of cysticerci of T. cf. krabbei as adult cestodes in experi-
mentally infected dogs was high, with 7 of 7 cysticerci maturing to adult
worms in one dog. An average of 9.2–9.3 proglottids, with an average of
19,300 eggs each, were shed per day throughout patency that lasted at least
131 days. Ten sheep, seven goats, one domestic calf and two pigs were
refractory to experimental infection with T. cf. krabbei of reindeer origin,
suggesting host specificity of this parasite (Sweatman and Henshall, 1962).
Sweatman and Plummer (1957) conducted similar studies on the life
history of T. hydatigena. The prepatent period in dogs experimentally
infected with cysticerci from sheep or moose was 51–76 days and patency
lasted 4.5–11.5 months. During that time, proglottids were excreted regu-
larly with one dog infected with five worms excreting an average of 3.7
proglottids per day. Excreted proglottids contained from 6000–23,000 eggs
and some remained active for a day or so post-excretion and were highly
mobile, moving up to three feet from the faeces (Sweatman and Plum-
mer, 1957). In contrast to T. krabbei, T. hydatigena of moose origin, passaged
through a dog, was infective to domestic sheep, suggesting no species bar-
riers between the sylvatic and domestic cycle for this species (Sweatman
and Plummer, 1957).
In contrast to domestic sheep, cysticerci in moose, reindeer and mus-
koxen can mature in the parenchyma of the liver (Choquette et al., 1957;
Sweatman and Plummer, 1957; Gibbs and Tener, 1958). Cysticerci in the
liver parenchyma of moose remain viable for up to 48 hours at subzero
temperatures in northern Ontario, considerably longer than those on the
liver surface or in the omentum. Thus, development to mature, viable cys-
ticerci deep in the hepatic parenchyma may be a mechanism that enhances
transmission potential during the arctic winter in the sylvatic cycle (Sweat-
man and Plummer, 1957).
Adult stages of both T. cf. hydatigena and T. cf. krabbei have been
reported in domestic dogs (Canis familiaris), wolves (Canis lupus), coy-
otes (Canis latrans), red fox (Vulpes vulpes) and arctic fox (Vulpes alopex)
(Kapel and Nansen, 1996; Lavikainen et  al., 2011). Taenia cf. krabbei has
also been reported in black (Ursus americanus), brown (U. arctos) and polar
(U. maritimus) bears (Choquette et  al., 1969; Pence et  al., 1983; USNPC,
2011). To date, T. arctos has been described only from brown/grizzly bears
(Haukisalmi et al., 2011) but previous records of T. krabbei in ursids need to
be revisited. It is probable that the contribution of each intermediate and
definitive host species to the circulation of these cestodes in arctic environ-
ments differs. For example, in west Greenland and Svalbard where wolves
are absent and domestic dogs are few, it is the arctic fox that is responsible
Parasites in Ungulates of Arctic North America and Greenland     171

for maintaining T. krabbei (Bye, 1985; Kapel and Nansen, 1996; Stien et al.,
2010) whereas wolves may play a more important role elsewhere.
(c) Impacts: Taenia species are relatively common in arctic ungulates at
low intensities and in general do not seem to cause significant pathology.
There are, however, occasional hunter reports of animals in poor condi-
tion that are severely affected with T. cf. krabbei (Kutz, 2007). Migrations
of T. hydatigena through the liver can also cause tissue damage (Sweatman
and Plummer, 1957). In cross-sectional studies, there was no relationship
between the number of cysts of T. cf. hydatigena in the livers of caribou
and kidney fat index (Pollock et  al., 2009) and no detectable impact of
T. cf. hydatigena or T. cf. krabbei on body condition in moose (Addison
et al., 1979).
Taenia hydatigena, T. krabbei and T. arctos are not known zoonoses; how-
ever, T. krabbei and T. arctos are sister species of T. multiceps and T. solium,
respectively, both of which can infect people, leading to uncertainty con-
cerning the zoonotic potential for these arctic taeniids (Lavikainen et al.,
2008). Meat or livers with high intensities of cysticerci may be discarded
by harvesters (Kutz, 2007; B. Elkin, S. Kutz, unpubl. obs.). Subfamily Echinococcinae Echinococcus granulosus

(a) Host and Geographic Distributions: Echinococcus granulosus occurs in
the larval stage (hydatid cysts) in the lungs of reindeer, caribou, moose
and muskoxen across North America (Table 2.6) (Gibbs and Tener, 1958;
Rausch, 1967; Choquette et  al., 1973; Barrett and Dau, 1981; Rausch,
2003). It is reported in mountain goats from temperate regions (Foreyt
et al., 2009) but has not been found in Dall’s sheep nor is it known from
Greenland (OIE, 1998; Smith, 1957 in Rausch, 2003). Two strains circulate
in ungulates of arctic Canada, G8 and G10, and these differ from other
forms of E. granulosus with respect to pathogenicity to people, infectiv-
ity to domestic ungulates, serology and genetics (reviewed in Thompson,
2008). Whether these strains represent a different species of Echinococcus,
that is, E. canadensis, is unresolved (Thompson, 2008; Knapp, 2011).
(b) Ecology. Wolves (Canis lupus) are the primary definitive hosts in the
Arctic and coyotes (Canis latrans) and domestic dogs can also be infected
(Rausch, 2003). The prepatent period is 56–65 days in dogs, maximum egg
production occurs as early as 76 days post-infection, and the lifespan of the
adult parasite is 8 months to a year (Sweatman and Williams, 1963; Rausch,
1993). Individual dogs can acquire hundreds to tens of thousands of adult
parasites following ingestion of hydatid cysts (Rausch, 1993). Ungulates
are infected by ingestion of eggs from the faeces of infected canids. Like
species of Taenia, these eggs can persist in the environment under cool
172     Susan J. Kutz et al.

moist conditions (Gemmel, 1977). In caribou and moose prevalence, inten-

sity and cyst size increase significantly with age and up to 167 cysts have
been reported in a single moose (Addison et al., 1979; Thomas, 1996). Echi-
nococcus granulosus is zoonotic, and exposure to faeces from infected dogs
that have consumed cysts in wild game is a potential risk in arctic com-
munities (Choquette et  al., 1973; Rausch, 2003; Himsworth et  al., 2010).
Skinning wolves and foxes are also potential zoonotic risks for trappers.
(c) Impacts. In arctic ungulates, hydatid cysts are found predominantly
in the lungs and less frequently in the liver where they are usually abnor-
mal and sterile (Rausch, 2003; Broughton et al., 1967). In moose, they can
also occur in the spleen, heart or kidneys (Addison et al., 1979). Thomas
(1996) was unable to detect a significant impact of E. granulosus on preg-
nancy, weight or kidney fat in caribou although there were trends towards
poorer body condition and lower pregnancy rates. Infection in moose may
lead to increased mortality; those with high burdens of cysts in their lungs
are more susceptible to hunting and predation than are those with low
burdens or no infection (Rau and Caron, 1979; Joly and Messier, 2004). The
impacts in other arctic ungulates are unknown.

2.4.2. Ungulates as definitive hosts: Anoplocephalidae Subfamilies Anoplocephalinae and Thysanosomatinae Moniezia, Avitellina, Thysanosoma

(a) Host and Geographic Ranges: Moniezia and Avitellina are large, long ces-
todes reaching several metres in length and found in the small intestine of
ruminants. Eggs of anoplocephalid tapeworms have been recovered from
faeces of muskoxen, Dall’s sheep, caribou and mountain goats through-
out most of their range (Table 2.6). Adult specimens of Moniezia expansa
have been reported from muskoxen in NU and NT (Gibbs and Tener, 1958;
Tener, 1965; Samuel and Gray, 1974). Anoplocephalid eggs are present in
the faeces of muskoxen in Nunavik, QC, and may differ morphologically
from those recovered from muskoxen in the western Canadian Arctic
(S. Kutz, M. Simard, unpubl. data). Thysanosoma actinoides and M. expansa
are reported in moose from temperate regions of North America (Samuel
et al., 1976; Stock and Barrett, 1983; Hoeve et al., 1988) and anoplocephalid
eggs are common in moose from the arctic and subarctic regions (Table 2.6).
Moniezia sp. is reported from Dall’s sheep of the Mackenzie Mountains
(Simmons et al., 2001) and M. benedeni, Avitellina sp. and Thysanosoma acti-
noides are reported in mountain goats from western Canada (Cowan, 1951;
Samuel et al., 1977).
The diversity of anoplocephalid cestodes in subspecies of Rangifer is
not well documented in North American and Greenland. Avitellina arctica
was reported in a caribou from the Thelon Game Sanctuary, NT (Gibbs,
Parasites in Ungulates of Arctic North America and Greenland     173

1960) and the Rivière-George caribou herd in QC in 2006 (USNPC, 2011)

and is commonly reported from reindeer in Eurasia. Several species of
Moniezia including M. benedeni, M. taimyrica and M. rangiferina have been
described in reindeer from Russia, Norway and South Georgia Island
(Semenova, 1967; Zelinskii, 1973; Leader-Williams, 1980; Bye, 1985); how-
ever, there are no confirmed reports of Moniezia sp. in free-ranging arctic
and subarctic North American caribou. Diversity of anoplocephalids, and
particularly species of Moniezia at high latitudes, requires further inves-
tigation including the application of new molecular-based methods to
unequivocally resolve identity and host associations for these otherwise
widespread species.
(b) Ecology. Anoplocephalids have an indirect life cycle. Eggs in the fae-
ces of infected ungulate definitive hosts are ingested by arthropod inter-
mediate hosts where they develop to the infective cysticercoid stage. The
life cycle is completed when cysticercoids are ingested by the definitive
hosts. Moniezia spp. are generally transmitted by oribatid mites (Samuel
and Gray, 1974; Elliott, 1986; Denegri, 1989; Xiao and Herd, 1992) and in
Russia Avitellina arctica develops in at least two species of Collembola,
Onychiurus taimyricus and O. furcifera (Kozlov, 1986). Development to fully
formed cysticercoids is temperature dependent, for example, ranging
from 27 (28°C) to 97 (18–20°C) days for M. expansa in oribatid mites (Nar-
sapur and Prokopic, 1979). The long development time at these relatively
warm temperatures (18–20°C) is perhaps surprising for an arctic parasite
and suggests that climatic conditions may play an important role as deter-
minants of geographic range and epidemiology of this group of parasites.
Anoplocephalids are generally parasites of young animals and are
uncommon in adults (Kirilenko, 1975; Bye, 1985). There is some evidence
of host specificity, for example, A. arctica does not infect ‘horned’ species
that are sympatric with infected cervids in Russia (Gibbs, 1960). Similarly,
caribou that are sympatric with infected muskoxen in the Thelon Game
Sanctuary, NU, were infected with A. arctica while M. expansa was identi-
fied from muskoxen (Gibbs and Tener, 1958; Gibbs, 1960).
(c) Impacts. Anoplocephalid tapeworms can cause diarrhoea and
reduced weight gain in domestic lambs (Narsapur, 1988). In reindeer in
Russia, A. arctica causes sufficient pathology in calves to warrant treatment
and M. baeri, M expansa and M. benedeni are reported to cause unthriftiness
and emaciation (Polyanskaya, 1961; Kirilenko, 1975). For muskoxen, there
is some evidence of pathology induced by Moniezia spp. Translocated
muskox calves that grazed on pasture previously occupied by domestic
sheep and cattle in Iceland died with heavy tapeworm infections and
scouring in captive muskoxen in Norway was attributed to Moniezia spp.
(Samuel and Gray, 1974). The specimens of Moniezia were not identified to
species in either of these cases.
174     Susan J. Kutz et al.

TABLE 2.7  Trematodes reported from ungulates of arctic North America, including
Greenland. The range of prevalence reported is indicated below the parasite name. Only
prevalence estimates based on sufficient sample sizes are included. Data compiled from
available published and grey literature

Host and Parasites Herd or location

Fascioloides magna QC Rivière-aux-Feuillesa; Rivière Georgeb–d
Paramphistomum cervi AK Cantwelle; Northern Alaska Peninsula, Mulchatnaf
Fascioloides magna (87%) QC Kuujjuak, Tasiujaqg
Paramphistomum cervi AK Anchorageh; Fairbanks, Tanana Flatsf
a  Ducrocq and Lair (2007).
b  Choquette et al. (1971).
c  Parker (1981).

d  Lankester and Luttich (1988).

e  Dieterich, (1981).

f  K. Beckmen (unpubl. obs.).

g  M. Simard (pers. comm.).

h  USNPC, (2011).

FIGURE 2.10  Trematoda reported from ungulates of arctic North America, including

2.4.3. Emerging issues and knowledge gaps for the Cestoda

Cestoda, although widespread in ungulates of arctic North America and
Greenland, are not well characterized. Recent phylogenetic work on the
taeniids, together with discovery of a new species of Taenia circulating in
moose across the Holarctic, highlights the possibility of additional cryptic
species and complexes circulating in ungulates from the Arctic and Sub-
arctic (Lavikainen et al., 2008; Lavikainen et al., 2010; Haukisalmi et al.,
2011; Lavikainen et al., 2011).
Similarly, for the anoplocephalids, the Russian literature suggests that
there may be considerable hidden diversity within Moniezia, that anoplo-
cephalids may have significant impacts on their hosts and that they may
Parasites in Ungulates of Arctic North America and Greenland     175

be influenced by climate changes (Priadko, 1976; Narsapur and Prokopic,

1979). That there has been no recent work on biodiversity or impacts of
this family in North America is perhaps surprising. Further characteriza-
tion of the cestode fauna of arctic ungulates is warranted and will strongly
benefit from molecular approaches in defining species limits, diversity and
epidemiological patterns. There is also a need to more critically explore
the impacts of these parasites in arctic hosts, their potential zoonotic risk,
particularly for taeniids, and how they circulate among the various defini-
tive and intermediate hosts.


The trematode fauna of ungulates in arctic North America is very

simple, consisting of only two known species: Fascioloides magna, the
giant liver fluke, and Paramphistomum cervi, the rumen fluke (Table 2.7,
Figure 2.10). Both parasites require aquatic snails as intermediate hosts for

2.5.1. Family Fasciolidae Subfamily Fasciolinae Fascioloides magna

(a) Host and Geographic ranges: The arctic distribution of F. magna is limited
to caribou and muskoxen from northern Quebec and Labrador (Choquette
et  al., 1971; Lankester and Luttich, 1988; Pollock et  al., 2009: M. Simard
pers. comm) (Table 2.7). Both hosts become patent and prevalence is high,
often approaching 100%. Moose are dead-end hosts for F. magna (Pybus,
2001), and it has not been reported in mountain goats or Dall’s sheep nor
has it been reported in Greenland.
(b) Ecology: Aquatic snails of the family Lymnaeidae are intermediate
hosts for F. magna (Pybus, 2001; Králová-Hromadová et al., 2011). Lym-
naeid snails are present across the Arctic (Hershey, 1990) and various
stages of the parasite have been demonstrated to overwinter in snails
(Pybus, 2001). In caribou, prevalence and intensity tend to increase
with age (Lankester and Luttich, 1988). The life cycle in muskoxen is
(c) Impacts: Fascioloides magna causes substantial liver pathology
in normal and aberrant hosts (Pybus, 2001). In caribou, adult flukes
are associated with lesions that include fibrous capsules typically con-
taining two flukes and copious amounts of viscous grey–brown/black
fluid. Migrating immature flukes are associated with blood filled tun-
176     Susan J. Kutz et al.

nels up to 1.5cm wide (Lankester and Luttich, 1988). Similar lesions are
present in muskoxen (CCWHC, 2011). Despite the significant hepatic
damage, there is no evidence that F. magna has negative effects on
body condition of caribou (Lankester and Luttich, 1988; Pollock et al.,
2009). In moose, the flukes do not mature and the continued migra-
tion of immature flukes through the liver can lead to mortality (Pybus,
2001). Flukes also did not mature in three bighorn sheep experimentally
infected with 50 or 100 metacercariae. All three sheep died from the
effects of the flukes within 104–197 days post-infection. Post-mortem
findings included multifocal pyogranulomatous hepatitis, necrotiz-
ing haemorrhagic pneumonia, pleuritis and peritonitis (Foreyt, 1996).
Three, 18 and 21 flukes were recovered from the sheep indicating a
low lethal dose. A similar outcome might be expected in other bovids,
specifically Dall’s sheep and mountain goats. The introduction of
F. magna into areas where hosts had not been previously exposed is
related to mortality events in European cervids (Balbo et  al., 1989;
Slavica et al., 2006).
Fascioloides magna is present in wild cervids of northern BC, AB and
SK (Wobeser et al., 1985; Pybus, 2001) but its distribution is patchy. Range
expansion for this parasite has been associated with natural migration
or translocation of infected hosts into non-endemic areas (Wobeser et al.,
1985; Pybus, 2001; Slavica et  al., 2006; Králová-Hromadová et  al., 2011).
Development in snail hosts is temperature dependent which may limit its
northward range expansion; however, it is well established in arctic Que-
bec, and the ability to overwinter in snails may facilitate its maintenance
in this environment.

2.5.2. Family Paramphistomidae Subfamily Paramphistominae Paramphistomum spp.

(a) Host and Geographic ranges: Paramphistomum spp. are rumen flukes that
are pear-shaped worms characterized by a large terminal ventral sucker.
Numerous genera and species within the Paramphistominae have been
described but the genus was redefined and restricted with only nine spe-
cies being retained (Eduardo, 1982). In North America, P. cervi is reported
in Alaskan caribou and moose (Dieterich, 1981; USNPC, 2011; K. Beckmen,
unpubl. data) and P. cervi and P. liorchis are known in moose from temperate
Canada (Lankester et al., 1979; Kennedy et al., 1985). Paramphistomum has
not been observed in muskoxen, Dall’s sheep or mountain goats. Param-
phistomum leydeni is documented in reindeer from Eurasia (Nikander, 1992).
(b) Ecology: The life cycle of species of Paramphistomum requires aquatic
snail intermediate hosts of which members of the Lymnaeidae and Planor-
Parasites in Ungulates of Arctic North America and Greenland     177

bidae are suitable (DeWaal, 2010). Miracidia develop in eggs, hatch, infect
aquatic snails and develop to cercaria. This process is temperature depen-
dent, and in one experimental study on P. cervi, miracidia developed in 20
days in eggs maintained at 20°C but did not hatch at temperatures below
13°C. When infected snails were maintained at 20°C, cercaria were shed by
50 days post-infection (reviewed by Lankester et al., 1979). Snails can shed
cercariae for up to one year (Dinnik and Dinnik, 1957). Based on the sea-
sonal variation in size of adult P. cervi throughout the year, Lankester et al.
(1979) proposed a one-year life cycle for parasites in moose from Ontario.
Animals are infected in the summer and flukes mature by the following
spring, breed and die by autumn. Maturation of flukes in moose appears
to be much slower than that in cattle, sheep and roe deer in Germany and
may be related to changing seasonal diet as well as a strategy to synchro-
nize egg production with availability of intermediate hosts in the summer
(Lankester et  al., 1979). In moose in Ontario, prevalence increased from
calves (14%) to yearlings (50%) to adults (82%) (Lankester et al., 1979).
Little is known about the effects of rumen flukes in wild cervids.
Heavy infections have been noted in severely debilitated adult moose and
caribou in AK (K. Beckmen, unpubl. obs.). There is one report of severe
denudation of rumen villae in heavily infected moose calves (Seyfarth,
1938 cited in Lankester et al., 1979). In general, clinical signs are uncom-

FIGURE 2.11  Protozoa reported from ungulates of arctic North America, including
178     Susan J. Kutz et al.

mon in domestic livestock but juvenile parasites in the small intestine may
cause a severe enteritis and profuse diarrhoea (DeWaal, 2010).
The host and geographic distribution of Paramphistomum flukes in
ruminants from the Canadian and Greenlandic Arctic remains virtually
unexplored, and the life cycle and effects are not well understood. Some
features of the life cycle for P. cervi, hatching only over 13°C, and long
development time for cercaria at 20°C in the snail intermediate hosts may
limit the abundance and distribution of this parasite at northern latitudes
(note though Paramphistomum spp. are widespread in reindeer of the Rus-
sian taiga). Species of Paramphistomum are typically considered parasites
of tropical regions, and recent increased occurrence in domestic livestock
at more northern latitudes (DeWaal, 2010) may reflect changes in geo-
graphic distribution, perhaps linked to climatic changes. Further survey
and inventory in the Arctic should be pursued.


Arctic ungulates are host to a broad array of gastrointestinal and tissue

protozoa (Figure 2.11).

2.6.1. Protozoa of the gastrointestinal tract Family Hexamitidae Giardia duodenalis
Giardia is a genus of intestinal protozoa that infects a variety of vertebrate
hosts, including people and wildlife (Thompson, 2004). Giardia duodenalis
(synonyms: G. intestinalis and G. lamblia) infects a wide range of free-rang-
ing and domestic animals, and people (Thompson, 1998). A minimum of
seven assemblages (A–G) and many subgroups are recognized (Thomp-
son, 2004; Lasek-Nesselquist et al., 2010). Some subgroups of assemblage
A and B are zoonotic (Sprong et al., 2009). Other assemblages (C–G) are
considered host specific and non-zoonotic (Lebbad et al., 2010).
(a) Host and Geographic Distributions: Giardia species are reported with a
patchy distribution and low prevalence and intensity in caribou and Dall’s
sheep from North America (Table 2.8) (Samuel and Gray, 1974; Roach
et al., 1993; Siefker et al., 2002; Kutz et al., 2008; Kutz et al., 2009c). Giardia
duodenalis assemblage A is common in muskoxen on Banks Island, NT,
(Kutz et al., 2008) but absent from over 200 muskoxen tested on Victoria
Island, NT and NU (S. Kutz, J. Wu, S. Checkley, M. Dumond unpubl. obs.).
In a broad survey of frozen faeces from 520 barren-ground caribou from
twelve herds in North America, only seven sample(s) tested by immuno-
fluorescent antibody (Waterborne Inc.) were positive for Giardia (S. Kutz
Parasites in Ungulates of Arctic North America and Greenland     179

TABLE 2.8  Gastrointestinal protozoa reported in ungulates of arctic North America,

including Greenland. The range of prevalence reported is indicated beside the ­parasite
name. Herds or locations where the parasites were tested for but were absent are
­indicated by a ‘0’ following the location/herd with the number of animals tested
­following in parentheses. Data compiled from available published and grey literature

Host and parasite species

(range of prevalence) Herd, region or nearest place name

Caribou and reindeer

Cryptosporidium sp. (1.3–12%) AK Teshekpuk and Western Arctica
NT South Slave regionb; Banks Islandc
Giardia sp. (3%) AK Teshekpuk and Western Arctica
NT Banks Islandc
Eimeria sp. YT Chisanad
NT South Slaveb
Cryptosporidium sp. AK Colville River area 0(32) a
Giardia sp. AK Colville River area 0(32) a
Cryptosporidium sp. NT Banks Island 0(72) e
Giardia duodenalis Assemblage A NT Banks Islande
Eimeria sp. NU Devon Islandf
Eimeria moshati (75–100%) AK Nunavik Islandg
E. faurei (43–100%) NU Bathurst Islandg
E. ovina (93–100%) QC Kuujjuaq and Tasiujaqg
Eimeria granulosa (21 and 24%) AK Nunavik Islandg
NU Bathurst Islandg
Eimeria oomingmakensis (14.3%) NU Bathurst Islandg
Dall’s sheep
Cryptosporidium spp. YT Not specified 0(5) h
Giardia (40%) YT Not specifiedh
Eimeria ahsata NT Mackenzie Mountainsi,j
Eimeria crandallis NT Mackenzie Mountainsi,j
Eimeria dalli AK Kenai Peninsulak
NT Mackenzie Mountainsi,j
Eimeria ninakohlyakimovae NT Mackenzie Mountainsi,j
Eimeria parva NT Mackenzie Mountainsi,j
a  Siefker et al. (2002). i Uhazy et al. (1971).
b  Johnson et al. (2010). j Simmons et al., (2001).
c  Nagy et al. (1998). k  Clark and Coldell (1974).

d  Hoar et al. (2009).

e  Kutz et al. (2008).

f  Samuel and Gray (1974).

g  Duszynski et al. (1977).

h  Roach et al. (1993).

180     Susan J. Kutz et al.

and CARMA, unpubl. obs). Giardia was not found in a survey of 92 cari-
bou from two herds in western Greenland (S. Kutz, C. Cuyler, unpubl.
obs.) nor is it reported for other Greenland wildlife, but it was found in
Greenlandic people (Babbott et  al., 1961; Krasilnikoff and Gudmand-
Hoeyer, 1978). Giardia sp. have not been documented in moose from the
North American Arctic but are reported in moose from northern Saskatch-
ewan (Heitman et al., 2002) and G. duodenalis assemblage A are reported
from moose in Norway and Sweden and in reindeer in Norway (Heitman
et al., 2002; Siefker et al., 2002; Hamnes et al., 2006; Lebbad et al., 2010).
(b) Impacts: Clinical disease associated with Giardia spp. has not been
described in free-ranging arctic ungulates. In people and domestic ani-
mals, clinical signs can include diarrhoea, dehydration, abdominal pain
and weight loss (Thompson, 2004; Collinet-Adler and Ward, 2010). In
cattle, Giardia spp. infections and disease mainly affect calves and can
decrease herd performance (Naciri et al., 1999; Olson et al., 2004).
(c) Ecology: Giardia is typically considered a waterborne parasite but
transmission may be equally likely through contaminated vegetation
(Thompson, 2004). Giardia cysts are immediately infective and in general
are thought to be environmentally resistant (Thompson, 2004) but mul-
tiple freeze–thaw cycles may cause high mortality (Robertson and Gjerde,
2004; Robertson and Gjerde, 2006).
The high prevalence of G. duodenalis in muskoxen on Banks Island, NT,
demonstrates that it is capable of persisting in a true arctic environment.
The mechanisms for this persistence are unknown but could include over-
winter survival in both the hosts and the environment; cysts are docu-
mented in muskox faeces in winter (Kutz et al., 2008).
It is enigmatic that Giardia appears to be absent from muskoxen on the
adjacent Victoria Island while it is so well established on Banks Island.
Muskoxen on these islands presumably originated from a common Berin-
gian population; however, they have undergone bottlenecks in more
recent times (Gunn et  al., 1991b) that may have led to regional extirpa-
tion of Giardia in small sub-populations. Recognizing that the source of
infection could be people, the historical movements of Inuit, whalers and
explorers, and more recently tourists, must also be considered. A point
source introduction of Giardia by people to Banks Island, with subsequent
establishment and spread in the muskox population, is plausible. Con-
temporary ecological conditions on the islands also differ, with histori-
cally a higher density of muskoxen on Banks Island and perhaps a higher
concentration of animals around key water and food sources such as river
Our understanding of the epidemiology and transmission pathways
for Giardia spp. on Banks Island and elsewhere in the Arctic is limited by
patchy surveys and absence of ecological studies. Of particular interest is
the potential interaction among people, wildlife and domestic animals for
Parasites in Ungulates of Arctic North America and Greenland     181

the circulation of Giardia in northern ecosystems (Kutz et al., 2008; Kutz

et  al., 2009c). Giardia occurs in people, particularly the young, in arctic
communities (Babbott et al., 1961; Eaton and White, 1976) and has been
isolated from water sources for rural villages in Alaska (Pollen, 1996). Fur-
ther survey and strain characterization, in animals and people, are essen-
tial to better understand the ecology and potential impacts of this zoonotic
pathogen in wildlife and people in the Arctic. Family Cryptosporidae Cryptosporidium spp.

Cryptosporidium spp. are gastrointestinal protozoa that are important
causes of diarrhoea in people and a wide variety of animals (Fayer et al.,
2010). There are multiple species and genotypes and a range of host speci-
(a) Host and Geographic Distribution: Cryptosporidium spp. are occasion-
ally reported from muskoxen and caribou in the North American Arctic
and Subarctic (Table 2.8). They were not detected in over 80 caribou from
the Kangerlussuaq-Sisismiut and Akia-Maniitsoq caribou herds of west
Greenland (S. Kutz, C. Cuyler, unpubl. obs.) nor in faecal surveys from
moose in AK or Dall’s sheep in the YT (Roach et al., 1993; Siefker et al.,
2002; Kemper et al., 2004; Kutz et al., 2008). However, clinical disease asso-
ciated with Cryptosporidium was recently observed in one of two orphaned
moose calves in AK (K. Beckmen, R. Gerlach, unpubl. obs.) (Table 2.8).
A novel caribou genotype was reported from one herd of caribou in AK
(Siefker et al., 2002) and the isolates from the AK moose calves are cur-
rently being described (L. Ballweber, K. Beckmen, unpubl. obs.).
(b) Ecology: Based on fairly extensive faecal survey, Cryptosporidium is
not a common parasite of caribou, moose or muskoxen. Freezing can kill
Cryptosporidium spp. oocysts in laboratory conditions (Fayer et al., 2000)
and in colder aquatic and terrestrial environments; thus, transmission
may be temperature limited in the Arctic (Robertson and Gjerde, 2004;
Robertson and Gjerde, 2006).
(c) Impacts: Cryptosporidium is generally considered a disease of neo-
natal and young animals and tends to be self-limiting in immunocom-
petent hosts (Naciri et  al., 1999; Hamnes et  al., 2006; Petry et  al., 2010).
Clinical disease in wild arctic ungulates, other than a single moose calf
in AK, has not been reported, but Cryptosporidium spp. infection was the
cause of severe diarrhoea and lethargy in captive muskox calves in Sas-
katchewan, Canada (Western College of Veterinary Medicine, Saskatoon,
Saskatchewan medical records). The caribou genotype described from
AK is closely related to C. andersoni, an abomasal species associated with
182     Susan J. Kutz et al.

decreased milk production and lower weight gains in cattle (Ralston et al.,
2011); similar effects may be anticipated in caribou (Siefker et al., 2002). Family Eimeriidae Eimeria spp.

The Eimeriidae consists of a broad diversity of protozoal parasites of the
gastrointestinal tract. There have been some recent advances in knowl-
edge of species diversity in the Palaearctic ungulates, but little is known
about the ecology of this group of parasites in arctic ungulates.
(a) Host and Geographic Distributions: Eimeria species are found in almost
all examined caribou, muskoxen and Dall’s sheep populations throughout
their ranges in North America, including Greenland (Tables 8, 11). There is
a minimum of six species of Eimeria described from muskoxen and three
from Dall’s sheep (Uhazy et al., 1971; Clark and Coldell, 1974; Duszynski
et al., 1977; Korsholm and Olesen, 1993).
Perhaps surprisingly given the presumed host specificity of most
Eimeria species, three species from muskoxen, E. granulosa, E. ovina and
E. faurei, are also reported from bighorn sheep (Duszynski et  al., 1977).
The species of Eimeria in caribou of North America and Greenland have
not been identified, but Eimeria mayeri (prevalence 2.6%; n = 195), E. ran-
giferis (1.0%; n = 195) and E. hreindryria (1.8%; n = 56) have been described
in Icelandic reindeer (Gudmundsdottir and Skirnisson, 2005; Gudmunds-
dottir and Skirnisson, 2006), and E. arctica, E. mühlensi, E. tarandina and
Isospora rangiferis (the latter species identification may be suspect) have
been described in Russian reindeer (Yakimoff 1936, 1937 and 1939, cited
by Gudmundsdottir and Skirnisson, 2006). There are no reports of Eimeria
species in moose from northern BC, YK and NT but Eimeria sp. and associ-
ated diarrhoea in calves is a chronic problem in a captive, research herd of
moose in AK (K. Beckmen, unpubl. obs.) and E. alces has been described in
Russian moose (Soshkin, 1997).
(b) Ecology: Eimeria spp. of arctic ungulates have a direct life cycle
with oocysts shed in faeces, sporulation in the environment and infec-
tion through ingestion. In muskoxen, Eimeria oocysts are present in the
faeces year round, including throughout the winter (Table 2.11). Samuel
and Gray (1974) reported increased shedding of oocysts from muskoxen
in the high Arctic from March to June. At least some species of Eimeria
from muskoxen are freeze tolerant and sporulate after several months
storage at −20°C (R. Rember, S. Kutz, E. Greiner, unpubl. obs.). Sporula-
tion after extended freezing at −7°C or colder is rare for most Eimeria
spp. (Landers, 1953; Marquardt et  al., 1960; Rind and Brohi, 2001) but
ability to withstand freezing may be related to environmental conditions
under which the species exist. For example, Landers (1953) demonstrated
Parasites in Ungulates of Arctic North America and Greenland     183

sporulation of three species of Eimeria (E. arloingi, E. ninakohlyakintovi and

E. parva) from domestic sheep in Wyoming after freezing at −19 to −25°C
as well as repeated freeze–thaw cycles. These temperatures were simi-
lar to the extreme minimums for that region in winter. Other Eimeria of
cattle, E. bovis and E. zuernii sporulated after 24h of freezing at −20°C but
not when maintained for a longer time period (Rind and Brohi, 2001).
Freeze tolerance for Eimeria spp. from ­caribou and Dall’s sheep has not
been investigated.
The abundance of Eimeria spp. is low in barren-ground caribou but
quite high in both muskoxen and Dall’s sheep and the parasites tend
to be present year round in these latter species (Table 2.11). Such differ-
ences may reflect the different behaviour of these host species. Barren-
ground caribou have massive home ranges, migrate over vast distances
(over 1000 km) and are moving constantly throughout the summer
(Nagy et al., 2005). This behaviour may remove caribou spatially from
contaminated regions and reduce opportunities for exposure to infec-
tive oocysts. In contrast, muskoxen and Dall’s sheep are more seden-
tary with much smaller home ranges and a build-up of the parasites
in their immediate environment and ongoing exposure may be more
(c) Impacts: Clinical disease associated with Eimeria spp. is not common
in free-ranging arctic ungulates. The highest oocyst count reported in fae-
cal surveys of >1000 Dall’s sheep, caribou, moose and muskoxen in north-
ern Canada is 17,500 oocysts per gram (opg) of previously frozen faeces in
a muskox from Banks Island (NT) (Table 2.2). Oksanen et al. (1990) found
up to 350,000 Eimeria opg of faeces in reindeer calves and suggested that
clinical disease would be related to higher numbers of oocysts (>800,000
opg faeces) (Oksanen et  al., 1990). In Greenland, extremely high oocyst
counts (up to 990,000 opg) were recorded from calves during a mortality
event. The proximate cause of mortality was an E. coli septicaemia and the
role of Eimeria was not determined (Clausen et al., 1980).
(d) Issues and future research: Knowledge of Eimeria spp. in ungulates
of arctic North America is limited to primarily cross-sectional faecal sur-
veys and a few species descriptions. Survey data, a few case reports, and
preliminary laboratory experiments suggest differing patterns of infec-
tion and abundance among host species, possibly significant pathology
and arctic adaptations such as sporulation of oocysts after freezing. New
DNA-based technologies and morphological studies, together with fur-
ther observational (seasonal faecal surveys and characterization of para-
site diversity and abundance among host species and age/sex classes) and
experimental research are necessary to describe the species diversity, host
range, ecology and significance of Eimeria in the Arctic.
184     Susan J. Kutz et al.

2.6.2. Tissue and blood protozoa: the Sarcocystidae,

Trypansomatidae and Babesiidae Family Sarcocystidae
Besnoitia tarandi, Neospora caninum, Sarcocystis spp. and Toxoplasma gondii
are tissue-dwelling obligatory intracellular parasites of a variety of ver-
tebrate species, including arctic ungulates. The life cycle of these Sarco-
cystidae family members typically relies on predator–prey linkages with
predators as the definitive hosts. For some of these species, however,
vertical and horizontal transmission in the absence of definitive hosts
is possible. Diagnosis is by histological identification of cysts, immuno-
histochemistry, DNA-based techniques or serological tests (Dubey and
­Odening, 2001; Leighton and Gajadhar, 2001). Besnoitia tarandi

Besnoitia tarandi is a tissue cyst-forming parasite first described in Alaskan
reindeer in 1922 (Hadwen, 1922). Cysts are located in the skin, subcutane-
ous tissue, conjunctiva, sclera, periosteum of long bones and skull, muscle
fascia, testicles and occasionally other soft tissues (Ayroud et  al., 1995;
Wobeser, 1976). There are three other species of Besnoitia reported from
‘large mammal’ hosts and these include B. besnoiti, primarily from cattle,
B. bennetti primarily from domestic equids, and B. caprae primarily from
goats (Olias et  al., 2011). No significant genetic differences between B.
tarandi and B. besnoiti were identified in one study, but morphological and
biological differences suggested that further investigation with more pre-
cise genetic markers is needed (Olias et al., 2011). Subsequent work sug-
gests the utility of microsatellite markers in discriminating among such
taxa. Significant sampling has identified a stable multilocus genotype
for B. tarandi across the Arctic not precisely replicated in any of several
specimens of B. besnoiti heretofore examined (B. Rosenthal, pers. comm.).
Broader application of this and related methods might prove useful in
determining the duration and consequences of evolutionary differentia-
tion between these and related parasite taxa.
(a) Host and Geographic Distributions: Besnoitia tarandi has a circumarctic
distribution in Rangifer. In North America, it is present in semi-domestic
reindeer and free-ranging woodland and migratory barren-ground cari-
bou populations from AK to Labrador (Table 2.9). Prevalence on the main-
land tends to be higher than on nearby arctic islands and it is absent from
Greenland (Gunn et al., 1991a; Ducrocq, 2011). Rangifer species are the pri-
mary intermediate hosts; however, it has also been reported in muskoxen
on mainland Nunavut, Canada, but not in over 100 muskoxen sampled
on Victoria Island immediately to the north (Gunn et al., 1991a; J. Wu, S.
Kutz, S. Checkley, unpubl. obs.). It also occurs in reindeer in Fennoscan-
dia and Russia (Nikolaevskii, 1961; Rehbinder et  al., 1981; Dubey et  al.,
Parasites in Ungulates of Arctic North America and Greenland     185

TABLE 2.9  Tissue and blood protozoans reported from ungulates of arctic North
America, including Greenland. The range of prevalence reported is indicated below the
parasite name. Only prevalence estimates based on sufficient sample sizes and reliable
diagnostic techniques were included (e.g. data from cursory visual assessment for Sar-
cocystis and Besnoitia were excluded but histological assessment included). Locations/
herds where the parasites were tested for but were absent are indicated by a ‘0’ follow-
ing the location/herd and sample size ‘n’ following in parentheses. Data compiled from
available published and grey literature

Host and parasite species

(range of prevalence) Herd, region or nearest place name

Caribou or reindeer (rd)

Besnoitia tarandi (5–78%) AK Variousa; Western Arctic or Teshepukb;
NT Mackenzie River Delta (rd) d; Not
specified(rd) e; Cape Bathurstf; Bluenose
NU Bathurstc; Dolphin-Uniong; Southampton
QC Riviere-aux-Feuillesc; Riviere Georgec
Sarcocystis sp. (37.5–100%) AK Adak, Delta, Izembek, Nelchina, Porcupine,
Western Arctic, Wrangell Mountain h,
NT Bluenose West n
NU Victoria Islandg; Bathurstc
QC Riviere George and Feuillesc; Goose Bay and
Toxoplasma gondii AK North Slope and Alaska Peninsulak; ­Various,
(0.7–62.5%) Porcupine, Western Arcticl
YT Chisanam
NT Bluenose and Beverly n; southern NTac
NU Bathurst, Dolphin-Union, and North Baffin
QC Riviere George and Feuilleso,p
GL Akia-Maniitsoq 0(49); Kangerlussuaq-
Sisimiut 0 (50) q
Neospora caninum AK North Slope and Alaska Peninsulak;
(1.4–15.7%) ­Porcupine, Western Arctic, Variousl
YT Chisanam
NT Bathurstr
Trypanosoma sp. AK Fairbanks (reindeer from Nome) a
YT Porcupineab
NT South Slaveac
NU Bathurstab
GL Akia-Maniitsoq, Kangerlussuaq-Sisimiutab

186     Susan J. Kutz et al.

TABLE 2.9  (continued)

Host and parasite species

(range of prevalence) Herd, region or nearest place name
Dall’s sheep
Sarcocystis spp. (14–77.4%) AK Alaska Range, Brooks Range, McCumber
Creek, Sheep Creek, Tok, Wrangell
Mountainsh; Variousi
NT Mackenzie Mountainss
Toxoplasma gondii (6.9%) AK Interiork
Neospora caninum AK Various 0 (52) b
Trypanosoma sp. NT Mackenzie Mountainsae
Sarcocystis spp. AK Interior, Holitna River and Nelchina,
McKinley Park, Seward Peninsula, Stikine
River, Unit 13, White Riverh; Variousi
Toxoplasma gondii AK North Slope, Interior and South Central
(1.3–22.7) regionsk; South Central and Interior
regions 0(201)l
Neospora caninum (0.5–2.5) AK South Central and Interior regions 0(201)l;
Not specifiedt
NT Mackenzie Valley Sahtu Settlement Regionu
Trypanosoma sp. AK Not specifiedad
B. tarandi (32%) NU Kugluktukg; Victoria Island 0(153)v
Sarcocystis spp 80% AK Nunivak Islandh
NT Banks Islandw
NU Ellesmere Islandx
Toxoplasma gondii NT Victoria Island (Holman)y
(4.6–40%) NU Kugluktuk and Victoria Island (Cambridge
Neospora caninum (6–8%) AK Eastern North Slopeb; Not specifiedt
NU Victoria Island (Cambridge Bay)v
a  Hadwen (1922).
b  Beckmen (2010).
c  Ducrocq and Lair (2007), J. Ducrocq, S. Lair, CARMA (unpubl. obs).

d  Choquette et al. (1967).

e  Lewis (1992).

f  Larter (1999).

g  Gunn et al. (1991a).

h  Neiland (1981).

i  Dau (1981).

j  Khan and Evans (2006).

k  Zarnke et al. (2000).

l  Stieve et al. (2010).

Parasites in Ungulates of Arctic North America and Greenland     187

TABLE 2.9  (continued)

m  M. Oakley, S. Kutz, R. Farnell (unpubl. obs.).
n  Kutz et al. (2001d).
o  Leclair and Doidge (2001).

p  McDonald et al. (1990).

q  P. Curry, Susan Kutz, 2012 S. Kutz, C. Cuyler (unpubl. obs.).

r  P. Curry, S. Kutz, CARMA (unpubl. obs.).

s  Kutz et al. (2001a).

t  Dubey and Thullez (2005).

u  C. Kashivakura, S. Kutz, A. Veitch, J. Invik (unpubl. obs.).

v  J. Wu, S. Kutz, M. Dumond, S. Checkley (unpubl. obs.).

w  Tessaro et al. (1984).

x  Samuel and Gray (1974).

y  Kutz et al. (2000a).

aa  Kingston et al. (1982).

ab  D. Schock, S. Kutz, CARMA (unpubl. obs.).

ac  Johnson et al. (2010).

ad  Kingston (1985).

ae  S. Kutz, A. Veitch (unpubl. obs.).

2004; Ducrocq, 2011), and the status of free-ranging reindeer from Iceland
is unknown (R. Thorarinsdottir pers. comm.).
Diagnosis in free-ranging ungulates is typically through gross and his-
tological examination. In caribou, histological evaluation of skin from the
mid-cranial metatarsus for cysts provides a sensitive measure for preva-
lence and intensity of infection (Ducrocq et al. 2012). In the live animal,
hosts with high infection intensities can be identified by visual observation
of parasitic cysts on the ocular conjunctiva but this method significantly
underestimates the true prevalence (sensitivity of 0.29 and specificity of
0.98) (Ducrocq, 2011). A commercial serological assay is available for B.
besnoiti in domestic livestock (Schares et al., 2011) but has not been vali-
dated for B. tarandi or arctic ungulates.
(b) Ecology: The transmission cycle for Besnoitia spp. remains poorly
understood (see Olias et  al. 2011 for a review). Feline definitive hosts
have been confirmed for some of the Besnoitia spp. that have small animal
intermediate hosts (e.g. B. darlingi, B. wallacei, B. oryctofelisi, B. neotomofe-
lis); definitive hosts have not been identified for those with large animal
intermediate hosts (B. besnoitia, B. benneti, B. tarandi) (Olias et  al., 2011;
Basso et al., 2011). Specifically for B. tarandi, experimental infections of a
limited numbers of dogs, domestic cats, raccoons and an arctic fox were
unable to establish these species as definitive hosts (Glover et al., 1990;
Ayroud et al., 1995; Dubey et al., 2004). Possible alternate definitive hosts
that are present across the range of most affected herds include arctic fox
(Vulpes lagopus), wolverine (Gulo gulo), lynx (Lynx lynx) and wolf (Canis
188     Susan J. Kutz et al.

Transmission of Besnoitia sp. by insect vectors has also been hypoth-

esized and tabanids, mosquitoes, tse tse and stable flies were experimen-
tally demonstrated to be competent for mechanical transmission of B.
besnoiti among cattle and between cattle and rabbits (Bigalke, 1968; Olias
et al., 2011). Epidemiological evidence for B. tarandi supports the possibil-
ity of vector-borne transmission but does not rule out carnivore defini-
tive hosts. A study of risk factors associated with B. tarandi infection in
two herds in QC, Canada, demonstrated that the prevalence and inten-
sity of Besnoitia cysts in the metatarsal skin increased from summer to fall
of the same year suggesting summer transmission (Ducrocq, 2011). This
could have occurred as a result of vector-borne transmission but could
also be explained by the presence of a definitive host, which may be more
abundant, and contribute to more environmental contamination on the
summer range compared to the winter range. Vector-borne transmission
was also hypothesized in an outbreak in captive zoo animals that demon-
strated similar temporal patterns of occurrence (Glover et al., 1990).
Importantly, transmission of Besnoitia sp. through insects and defini-
tive hosts are not exclusive of each other. Other modes of transmission
have also been suggested, including migratory birds and the possibility
that large mammals are aberrant hosts and the parasite is really main-
tained by small mammalian intermediate hosts (Olias et  al., 2011). The
finding of Besnoitia cysts in tundra mice sympatric with infected reindeer
herds is interesting and raises a question as to how Besnoitia may be circu-
lating in these tundra systems (Nikolaevskii, 1961).
In a recent study of North American migratory caribou herds, Besnoitia
prevalence, based on histological examination of metatarsal skin, was esti-
mated between 5.5 and 44.2% and maximum cyst density was 13.1 cysts/
mm2 (Ducrocq, 2011). Prevalence in males was higher than in females, and
prevalence of infection increased in the first years of life and then decreased
with age (Ducrocq, 2011). Decreases in B. tarandi cyst density over the win-
ter were observed and may be the result of either the ­elimination of B.
tarandi cysts from the dermis during the winter, or of a lower winter sur-
vival rate of caribou heavily infected by B. tarandi (Ducrocq, 2011). Com-
plete cyst elimination, however, is not known for other Besnoitia sp. and
there is little evidence to support this from histological examination of
more than a thousand caribou where only a few necrotic cysts with associ-
ated inflammatory cells were observed (Ducrocq, 2011).
Although B. tarandi has a wide geographic distribution, significant dis-
ease outbreaks in free-ranging caribou have only been reported recently in
the Rivière-George and Rivière-aux-Feuilles caribou herds in QC and Lab-
rador, Canada (Kutz et al., 2009b; Ducrocq, 2011). The cause of this disease
emergence is not understood, but possible hypotheses include a recent
introduction of B. tarandi to a naïve population, changing environmental
conditions that have allowed increased transmission rates or an increase
Parasites in Ungulates of Arctic North America and Greenland     189

in animal susceptibility. Prior to 2007, there was only a single report of

Besnoitia in caribou in QC and this was in 1960 from a herd of unknown
geographical origin (CCWHC, 2011). There were no subsequent records
in the Canadian Cooperative Wildlife Centre (CCWHC) database until
2007 when clinical besnoitiosis emerged in the Quebec herds (Ducrocq
and Lair, 2007). Although the CCWHC data are based on passive surveil-
lance, Besnoitia is routinely reported as an incidental finding in caribou
in other regions of arctic North America and previous lack of detection
in QC suggests absence or very low prevalence. Besnoitia tarandi isolates
from North America apparently do not differ genetically from those in
Fennoscandia (B. Rosenthal, pers. comm.) and may have been introduced
relatively recently to North America through multiple reindeer importa-
tions, primarily to AK, at the turn of the 20th century. Alternatively, this
uniformity may reflect the continuous distributions for Rangifer between
Eurasia and Beringia most recently during the Pleistocene and rapid geo-
graphic expansion in North America during the Holocene. The Rivière-
George and the Rivière-aux-Feuilles herds originate from the North
American lineage, south of the glaciers during the last ice age, and are
physically separated from other migratory caribou herds by Hudson Bay.
Thus, these herds may have been isolated from Besnoitia in both evolution-
ary and ecological time.
(c) Impacts: Clinical signs caused by B. tarandi in caribou range from
asymptomatic to significant clinical illness (Wobeser, 1976; Rehbinder
et al., 1981; Ducrocq and Lair, 2007). Severe pathology in captive caribou,
reindeer and mule deer (O. hemionus) was observed in an outbreak at the
Winnipeg Zoo where the naive status of the animals may have contrib-
uted to the severity of the infection (Glover et  al., 1990). Alopecia, skin
thickening, decreased mobility and resistance to movement are reported
for captive and free-ranging caribou with high infection intensities (Wobe-
ser, 1976; Rehbinder et  al., 1981; Ducrocq, 2011), and this may increase
susceptibility to predation and reduce thermoregulatory abilities. In
males, B. tarandi cysts can cause severe inflammation and obstruction of
blood vessels in the pampiniform plexus of the testicles (Choquette et al.,
1967; Wobeser, 1976; Ayroud et  al., 1995). Decreased or impaired fertil-
ity is reported in bovine and caprine besnoitiosis and this may also be
the case in Rangifer (Kumi-Diaka et al., 1981; Njenga et al., 1999). Testicu-
lar pathology can alter testosterone levels, causing antler malformation
and abnormalities (Blake et  al., 1998) that may influence social interac-
tions (Clutton-Brock, 1982) and reproductive success (Thomas and Barry,
2005). Velvet retention and broken antlers have been reported in caribou
infected with Besnoitia (Rehbinder et al., 1981; Ducrocq and Lair, 2007) and
further investigation of this association is warranted. Given the impact on
both survival and reproductive success, this parasite may play an impor-
tant role in population dynamics. Recent population surveys have shown
190     Susan J. Kutz et al.

substantial declines in the Rivière-aux-Feuilles and Rivière-George herds

within the past decades and the potential contribution of Besnoitia to these
declines is not known.
Besnoitia infection in muskoxen is rare but can cause severe pathology
including laminitis and ulcerative dermatitis (Gunn et al., 1991a). Limited
data suggest that infection in muskoxen is more prevalent on the main-
land compared to on arctic islands (Gunn et al., 1991a; J. Wu, S. Kutz, M.
Dumond, S. Checkley unpubl. obs.). The role of caribou in the epidemiol-
ogy of the parasite in muskoxen and other contributing factors for trans-
mission to muskoxen remain unknown.
(d) Issues and future research: Besnoitia tarandi is a common and wide-
spread parasite among subspecies of Rangifer across most of the Arctic.
Recent emergence of this parasite as a significant disease-causing agent
was surprising and highlighted the fact that we know very little about
its life cycle and epidemiology. The emergence of disease in Canadian
caribou coincided with emergence of B. besnoiti and associated disease
in domestic and wild animals in Europe (Mehlhorn et al., 2009), perhaps
raising the question of the possibility of a larger scale driver for the ecol-
ogy of this group of parasites. The lifecycles and epidemiology for both
B. tarandi and B. besnoiti remain virtually unknown, yet given the genetic
similarity between these two species, it follows that information gained
from one may guide the understanding of the other.
Priorities for future research on B. tarandi should include establishing
the parasite’s life cycle, likely a challenge considering that the life cycle of
B. besnoiti, a species with a much higher profile, has not yet been deter-
mined. Experimental studies together with epidemiological modelling
applied to existing data (e.g. Ducrocq, 2011) can be used to elucidate the
lifecycle of this parasite, evaluate the relative contribution of different
transmission pathways and understand the potential impacts of chang-
ing environmental conditions and animal communities on transmission
and disease. Apparent differences in disease occurrence and severity in
caribou and muskoxen across the Arctic, possibly related to differences
between individual hosts and/or host population susceptibility, and eco-
logical conditions, require further exploration. Impacts on individuals,
and how these translate to population-level effects, are important. Neospora caninum

Neospora caninum is best known as a parasite of agricultural economic
importance, causing abortion and neonatal mortality in cattle (Dubey
et al., 2007; Andreotti et al., 2010). In livestock, it is transmitted horizon-
tally through a canid-ungulate predator–prey life cycle and vertically
from mother to foetus. Its occurrence and potential significance in wildlife
are increasingly recognized.
Parasites in Ungulates of Arctic North America and Greenland     191

(a) Host and Geographic Distributions: Caribou, muskoxen and moose

seropositive for Neospora caninum are reported from AK, YT, NT and NU
(Table 2.9) but the parasite has not yet been isolated from these species.
None of 52 Dall’s sheep tested in AK between 1998 and 2004 were sero-
logically positive (K. Beckmen, unpubl. obs.). Wolves (n = 324, 9.0%) and
coyotes (n = 12, 16.7%), but not red foxes (n = 9), were seropositive in one
survey in AK (Stieve et al., 2010).
(b) Life Cycle: Canids are definitive hosts for N. caninum and a wide
variety of ungulates serve as intermediate hosts. Dogs and wolves are con-
sidered natural hosts, coyotes are demonstrated as suitable hosts experi-
mentally and N. caninum DNA, but not viable organisms, has been isolated
from the faeces of free-ranging coyotes and foxes (McAllister et al., 1998;
Gondim et al., 2004; Wapenaar et al., 2006; Dubey and Schares, 2011).
Seropositivity in remote caribou, moose and muskox populations in
various remote locations across the Arctic (Table 2.9), and competency
of wolves and coyotes as definitive hosts, provides compelling evidence
that N. caninum is a common parasite of sylvatic systems, perhaps pri-
marily, with spill-over to domestic agricultural systems. In many regions
of NT and NU, there are currently no domestic livestock and previous
introductions were limited to very few animals that were maintained in
the settlements by missionaries or traders for very short periods. Histori-
cally, working sled dogs may have been important in the life cycle as they
travelled extensively on the land and were fed wild game. Today, there are
very few working dogs and although these and non-working dogs are still
fed wild game (Salb et al., 2008; Brook et al., 2010), dog travel ‘on the land’
is not as common and opportunities for significant environmental con-
tamination may not be substantial. The few dogs that are brought into the
communities are typically small breeds that are (i) unlikely to have been
exposed to N. caninum previously and (ii) are unlikely to have any signifi-
cant travel outside the northern communities and limited opportunities,
therefore, to be a source of N. caninum for wildlife. Seropositive dogs have
been detected in two northern communities where wild game is a large
component of the diet for more than half of the dogs (Salb et al., 2008).
In caribou from YT and AK, there was no difference in Neospora serop-
revalence between calves and animals aged one year or older, suggesting
transplacental transmission (Stieve et al., 2010). Such a transmission route
may be important in maintaining the parasite under sub-optimal climatic
conditions and in regions with low densities of definitive and/or interme-
diate hosts. In one serological study on moose, exposure to Neospora was
detected but not common (Table 2.9) (Stieve et al., 2010). The low preva-
lence in moose was attributed to their feeding habits: they tend to browse
and eat aquatic vegetation, which could limit exposure to oocysts from
carnivore faeces (Stieve et al., 2010).
192     Susan J. Kutz et al.

(c) Impacts: Clinical signs associated with N. caninum have not been
reported in arctic ungulates, but this may reflect a lack of detection rather
than an absence of disease. The parasite was the cause of mortality in
a wild Californian black-tailed deer fawn (O. h. columbianus), causing
lesions in the lungs, liver and kidney (Woods et al., 1994), and transpla-
cental infection with N. caninum was reported in a stillborn captive Eld’
deer (Cervus eldi siamensis) in Europe (Dubey et  al., 1996). In domestic
cattle, N. caninum reduces fertility and causes abortion (Dubey and Lind-
say, 1996; Andreotti et al., 2010) and similar impacts are hypothesized in
free-ranging cervids (Dubey et al., 1996). There is anecdotal evidence that
Neospora may be linked to abortion in captive reindeer. Ninety-two per-
cent seroprevalence for Neospora was observed in a captive reindeer herd
approximately five months after a severe late-term abortion storm. Of the
39 animals (25 females, 14 males) in the herd, only three (two males, one
female) were found to be seronegative (Curry, 2010). The herd also had
a history of multiple pasture intrusions by coyotes during the ­summer
preceding the abortion storm. Unfortunately, no sera were available from
before the abortion storm to evaluate Neospora exposure (S. Kutz, K.
Orsel, P. Curry unpubl. obs.). Also, seroprevalence for Neospora was 15.8%
in adult females of a declining woodland caribou herd in the YT where
poor early calf survival was considered a major cause of the decline (M.
Oakley, S. Kutz, A. Seller, R. Farnell unpubl. obs.). There were anecdotal
reports of a late-term foetus/stillborn calf and additional weak calves in
the herd in the same year, but the potential contribution of Neospora was
not ­determined.
(d) Issues and future research: Serological investigation for N. caninum
in arctic ungulates has only been done in recent years and the full extent
of its host and geographic distribution in the Arctic is not well defined.
Isolation of the parasite from definitive and intermediate hosts should
be a priority in order to further characterize and compare these isolates
to those circulating in domestic cycles. It is probable that N. caninum has
reproductive impacts on caribou and other arctic ungulates that could
lead to substantially reduced productivity (i.e. abortion and stillbirths)
but low detectability of carcasses, thus resulting in ‘silent’ population
Finally, the relative role of different definitive host species (coyotes,
wolves and perhaps foxes and domestic dogs) as well as the contribution
of vertical transmission to maintenance of the parasite in wild host popu-
lations in the Arctic requires further exploration. Climate and landscape
change-related shifts in carnivore communities, such as northern range
expansion of coyotes, may alter the transmission dynamics of the para-
site depending on relative suitability of each of these definitive hosts. The
potential role of red and arctic foxes should also be considered.
Parasites in Ungulates of Arctic North America and Greenland     193 Toxoplasma gondii

Toxoplasma gondii is a pathogenic tissue cyst-forming protozoan with a
global distribution (Dubey and Beattie, 1988). It can cause abortions, foe-
tal abnormalities and neurological disease in a wide range of intermedi-
ate hosts, including people (Dubey and Beattie, 1988). Felids are the only
known definitive hosts for T. gondii but there is a broad range of inter-
mediate hosts (Sibley et al., 2009). Infection of intermediate hosts can be
through ingestion of sporulated oocysts that are shed in the faeces of felids,
transplacental transmission or carnivory. Toxoplasma gondii cysts develop
predominantly in neural and muscular tissues of intermediate hosts. Most
T. gondii isolates can be genotyped into three major clonal lineages (types
I, II, and III) (Sibley et al., 2009).
(a) Host and Geographic Distributions: Toxoplasma gondii appears to be
well established in the Arctic. It has been reported from a variety of terres-
trial and marine mammals and birds, as well as people, around the Arctic
(Table 2.9) (McDonald et al., 1990; Oksanen et al., 1998; Zarnke et al., 2000;
Kutz et  al., 2001a; Dubey et  al., 2003; Prestrud et  al., 2010; Stieve et  al.,
2010; Elmore et al., 2011).
Seropositive barren-ground and woodland caribou, muskoxen, Dall’s
sheep and moose are reported from AK to Labrador and from the subarctic
to the arctic islands but not in Greenland (Table 2.9). Similar to Neospora,
the actual parasite has not yet been isolated from arctic ungulates. Prev-
alence of infection in muskoxen and caribou decreases at higher lati-
tudes, from the mainland to the Arctic Archipelago (Kutz et  al., 2001a),
and a similar latitudinal gradient is reported for polar bears on Svalbard,
Norway (Jensen et al., 2010). The lineages circulating in North American
arctic ungulates have not been defined.
(b) Ecology: The transmission of T. gondii in Arctic ungulates remains
somewhat enigmatic. Domestic cats are rare and those that are present are
almost exclusively indoors (Prestrud et al., 2010; Stieve et al., 2010). Thus,
with the possible exception of occasional environmental contamination
from kitty litter (e.g. landfills or sewage), it is unlikely that the domestic
cat contributes significantly to the life cycle of the T. gondii in the Arctic
(Zarnke et al., 2000; Prestrud et al., 2010). Lynx (Lynx canadensis) are pres-
ent in the low Arctic and the Subarctic and seroprevalence for Toxoplasma
in this species ranges from 15% to 44% in AK, NT, BC and QC (Zarnke
et al., 2000; (Labelle et al., 2001; Philippa et al., 2004; S. Kutz, R. Mulders,
B. Elkin, JP Dubey, unpubl. obs.). Thus, lynx may serve as definitive hosts
in these regions.
The presence of seropositive caribou and muskoxen on arctic islands
where domestic and wild felids are absent suggests an alternate mode of
transmission at higher latitudes. On the arctic island of Svalbard, a high sero-
prevalence in arctic foxes in the absence of definitive hosts is attributed to pre-
dation on infected migratory geese (Jensen et al., 2010; Prestrud et al., 2010).
194     Susan J. Kutz et al.

Reindeer have been known to eat lemmings, and active or passive exposure
to cysts through contaminated vegetation or ingestion of carrion may be pos-
sible sources of infection for arctic ungulates (Oksanen et al., 2000). Vertical
transmission, as can occur in domestic goats and sheep (Dubey, 1982; Rodger
et al., 2006; Camossi et al., 2010), is another potentially very important means
of infection in arctic ungulates that may allow persistence of Toxoplasma for
multiple generations in the absence of a definitive hosts.
Seroconversion to Toxoplasma gondii increases with age in many wild
animal species (polar bears, arctic fox, wolves and cervids) indicating
cumulative exposure or age-dependant behaviours (Kutz et  al., 2000a;
Prestrud et al., 2007; Ankerstedt et al., 2010; Jensen et al., 2010; Jokelainen
et al., 2010). Risk factors for T. gondii exposure in arctic ungulates remain
undefined, but for other species variations in diet and behaviour are
important (Aubert et al., 2010; Jensen et al., 2010).
(c) Impacts: Overt disease caused by T. gondii has not been reported in
free-ranging arctic ungulates, but clinical disease is observed in captive
settings. Two experimentally infected reindeer developed signs of depres-
sion, decreased appetite and haemorrhagic diarrhoea leading to fatal
enteritis in one animal (Oksanen et al., 1996). Transplacental transmission
of T. gondii and subsequent abortion have been reported for a captive mus-
kox and a captive reindeer (Crawford et al., 2000; Dubey et al., 2002). The
impacts of Toxoplasma at the population level remain unknown; however,
if abortion/stillbirth is a consistent feature of this parasite in arctic ungu-
lates, then it may have a significant impact on populations by reducing
lifetime reproductive success. As with Neospora, such an impact would be
subtle and difficult to detect (poor calving rates but no visible carcasses
littering the tundra) yet could have major consequences for population
growth and/or stability.
Toxoplasma in subsistence species may pose a significant zoonotic risk
to aboriginal people, particularly with some traditional food preparation
methods where meat is eaten raw or undercooked and cysts may not be
inactivated. In the past, when wild game formed the core of the diet, pri-
mary exposure to cysts in meat probably occurred at a young age and con-
tinued throughout life. More recently, consumption of wild game is not as
common or consistent, and for some may occur only on special occasions,
meaning that many individuals may not be exposed to the parasite until
later in life. Such shifts in behaviour could increase the chances of primary
exposure occurring during pregnancy with subsequent risk of congenital
(d) Issues and future research: Although T. gondii may be an important
pathogen of wildlife and people in the Arctic its transmission and impacts
in arctic ungulates, and potential transmission risks from ungulates to peo-
ple, are very poorly understood. In particular, its presence at high arctic
latitudes in the absence of typical definitive hosts suggests alternate trans-
Parasites in Ungulates of Arctic North America and Greenland     195

mission pathways that need to be explored (Prestrud et al., 2010). To fur-

ther elucidate the life cycle of T. gondii in the Arctic, parasite isolation and
genotyping, together with studies on virulence and ecology are needed.
Such activities will also provide an insight into the worldwide circulation
of strains and their virulence (Aubert et al., 2010; Prestrud et al., 2010).
Recent evidence from the marine system suggests that T. gondii is
increasing in prevalence (Jensen et  al., 2010). Similar studies tracking
trends of T. gondii in arctic ungulates do not exist, although widespread
survey did occur during International Polar Year (Parkinson, 2008).
Emerging threats that may shift the transmission dynamics for T. gon-
dii include a growing human presence in the Arctic that is coupled with
increased environmental contamination through sewage, including bal-
last from cruise ships, waste disposal and increased numbers of domestic
cats (Prestrud et  al., 2010). Additional threats under a warming climate
include northern range expansion of possible definitive hosts such as lynx
and cougars (Felis concolor) (Anderson et al., 2010). Sarcocystis spp.

(a) Host and Geographic Distributions: Sarcocystis spp. are common in Dall’s
sheep, caribou, moose, muskoxen, and mountain goats in the North
American Arctic, and were detected by gross examination in caribou of
Greenland (Orsel, Cuyler pers. comm). Species diversity in the Nearctic
is poorly defined (Table 2.9), with only Sarcocystis alceslatrans and S. ovalis
described in moose from AB, Canada (Colwell and Mahrt, 1981; Dahlgren
and Gjerde, 2008). The biodiversity of this genus is much better described
for arctic ungulates of the Palaearctic. Sarcocystis ovalis, as well as S. alces,
S. scandinavica and S. hjorti have been described in moose in Norway, and
S. gruehneri, S. rangi, S. tarandivulpes, S. hardangeri, S. rangiferi and S. tarandi
have been described in reindeer in Norway and Iceland (Gudmundsdottir
and Skirnisson, 2006; Dahlgren and Gjerde, 2007; Dahlgren et al., 2008a).
The extent of these species in ungulates of arctic North America is not
(b) Ecology: Sarcocystis spp. use carnivore definitive hosts and herbivore
intermediate hosts. Sexual reproduction occurs in the gastrointestinal tract
of the definitive hosts, and asexual reproduction in the vascular endothe-
lium of the intermediate hosts, leading to tissue cysts in skeletal and car-
diac muscle and the nervous system (Herbert and Smith, 1987). A single
intermediate host can be infected by several different species of Sarcocystis
at the same time (Dubey and Odening, 2001; Dahlgren and Gjerde, 2007).
Canids are definitive hosts of S. alceslatrans found in North American
moose and of at least two and three of the species found in Norwegian
moose and reindeer, respectively (Fayer et al., 1982; Colwell and Mahrt,
1983; Dahlgren et al., 2008b; Dahlgren and Gjerde, 2010a). Potential defini-
tive hosts in the North American Arctic include arctic and red foxes,
196     Susan J. Kutz et al.

wolves, coyotes, black bears, grizzly bears, cougars, lynx, wolverine and
dogs (Neiland, 1981; Mahrt and Colwell, 1980; Dau, 1981; Foreyt, 1989;
Khan and Evans, 2006; Dahlgren and Gjerde, 2010b) Avian scavengers
such as corvids, which are common in the Arctic, may also act as definitive
hosts for some species (Gjerde and Dahlgren, 2010). Sarcocystis spp. in arc-
tic ungulates are not considered zoonotic, but this aspect of their ­biology
has not been adequately investigated (Tessaro et al., 1994).
(c) Impacts: The impact of Sarcocystis for most arctic ungulates has not
been investigated, but clinical disease associated with Sarcocystis spp. has
been reported in other naturally and experimentally infected cervid spe-
cies. A captive white-tailed deer died, after a week of lethargy, from an
acute necrotizing pneumonia caused by Sarcocystis sp. infection (­Duncan
et  al., 2000). In Oregon, an epizootic in free-ranging mule deer fawns
reduced growth rate (Dubey and Kistner, 1985). Experimental infections
of elk fawns with Sarcocystis spp., including S. sybillensis and S. wapiti,
resulted in weight loss (Foreyt et  al., 1995) and experimental infections
of mule deer fawns with S. hemionilatrantis led to anorexia, weight loss,
pyrexia, weakness and death (Hudkins and Kistner, 1977).
In semi-domestic reindeer, infection with Sarcocystis is a cause of
meat condemnation in Fennoscandia and thus a source of production
loss (Dahlgren and Gjerde, 2007). Changes in protein, moisture and fat
content, as well as increased bacterial contamination, were reported for
buffalo meat infected with sarcocysts (Mostafa and Yasein, 2010), but no
changes in meat quality were reported for bovine meat infected with S.
cruzi (Daugschies et al., 2000). To date, Sarcocystis infection has not been a
cause of meat condemnation in commercial caribou harvests in northern
Canada (B. Elkin, unpubl. obs.).
(d) Issues and future research: The knowledge on Sarcocystis spp. in
ungulates of arctic North American and Greenland is scant. The zoonotic
potential and effects of Sarcocystis spp. on the quality and safety of meat
from game animals in the Arctic is of considerable local importance and
requires further work. The biodiversity, life cycles, host specificity and
impacts are poorly described. Similarly, the potential impacts and conse-
quences of northern range expansion of definitive and intermediate host
species and their Sarcocystis spp. require exploration. Family Trypanosomatidae Trypanosoma spp.

Trypanosoma spp. are blood-borne protozoans that parasitize a wide range
of vertebrates globally. They are transmitted by blood-feeding arthropods.
In tropical regions some species, for example, T. congolense, and T. cruzi can
cause severe clinical disease in livestock and people, respectively, whereas
Parasites in Ungulates of Arctic North America and Greenland     197

those species in ungulates of temperate and arctic North America are not
considered significant pathogens.
(a) Host and Geographic Distributions. Trypanosoma spp. are widespread
and common in free-ranging ungulates in North America (Kingston, 1981).
They have been morphologically identified as T. cervi, but differences in
biology and infectivity for different hosts, together with absence of molec-
ular characterization of the parasite from various hosts, raises some uncer-
tainty as to whether more than one species circulates in cervids across North
America. Trypanosoma cf. cervi have been detected in the blood of reindeer,
woodland caribou, moose (culture and PCR) and Dall’s sheep in AK, NT,
NU and Greenland (Table 2.9) (Bequaert, 1942; Kingston, 1981 ; Kingston
et al., 1982; Kingston et al., 1985; Lefebvre et al., 1997; Johnson et al., 2010).
Trypanosoma sp., consistent with T. cervi, was detected in a mountain goat
from Montana (Kingston, 1985) and, using amplification and sequenc-
ing of a 550 base pair segment of the 18SrRNA gene, Trypanosoma sp. has
been found in mule deer (SK), ranched elk (AB), Rocky Mountain bighorn
sheep (BC) and wood bison (NT) (D. Schock, S. Kutz unpubl. obs., methods
as per Noyes et  al., 1999). Based on blood cultures or microhaematocrit
­centrifugation concentration, the prevalence of Trypanosoma sp. in free-
ranging caribou is quite high 72–84% (Lefebvre et al., 1997; Johnson et al.,
2010). There are no reports in muskoxen, which might reflect a lack of sur-
veillance, or could be real and reflect reduced rates of attack on muskoxen
by potential vectors. Trypanosoma sp. in caribou is morphologically similar
to T. cervi, but experimental exposure of two elk to trypanosomes from
Alaskan reindeer did not result in infection (Kingston et al., 1982).
(b) Ecology. In North America, Trypanosoma spp. have been isolated
from deer flies, ticks (Amblyomma americanum) and horse flies (reviewed in
Lefebvre et al. 1997). At least 33 species of tabanid flies are reported in the
Arctic (Teskey, 1988) although the species transmitting Trypanosoma in this
region are unknown. Trypanosoma spp. are present in Greenland where
arthropod diversity is likely quite poor, and investigation of potential vec-
tors in this relatively simple system may provide valuable insight into
transmission (D. Shock, S. Kutz, C. Cuyler unpubl. obs.). Transplacental
transmission of T. cervi in mule deer is documented, but the frequency and
significance of this mode of transmission is not known (Kingston, 1982).
Prevalence of infection appears to be seasonal in reindeer and elk with
highest prevalence based on direct examination, not culture, during mid-
summer and much lower prevalence in the mid to late autumn (Kingston,
1981; Kingston et al., 1982). This summer peak may coincide with vector
abundance and thus enhance opportunities for transmission.
(c) Impacts. No clinical disease has been reported associated with Try-
panosoma in arctic ungulates or wild North American cervids (Kingston
et al., 1982; Kingston and Nikander, 1985).
198     Susan J. Kutz et al. Invasive protozoa

Babesia spp. are apicomplexan protozoans transmitted by ticks, and in the
mammalian hosts, they invade red blood cells to replicate. Natural infec-
tions with Babesia have not been reported in free-ranging arctic ungulates
of North America or Greenland; however, natural infections with Babesia
and significant disease are common in eastern Russia (Rehbinder, 1990).
Babesia odocoilei has been reported from captive woodland caribou, farmed
reindeer and captive muskoxen in the USA (Holman et al., 1994; Holman
et al., 2003; Schoelkopf et al., 2005). It is transmitted by Ixodid ticks but
other possible vectors have been hypothesized in Russia (Zhilyaev, 1977).
In its mammalian hosts, Babesia spp. can cause intravascular hae-
molysis, anaemia, haemoglobinuria and occasionally a secondary toxic
nephritis (Petrini et al., 1995). It almost invariably causes severe disease
in captive Rangifer, with all cases of untreated babesiosis reported in
North American acute and fatal (Holman et  al., 1994; Schoelkopf et  al.,
2005; Bartlett et al., 2009). It is not known if subclinical babesiosis occurs
in caribou and reindeer (Schoelkopf et al., 2005), as has been observed in
farmed elk (Gallatin et al., 2003) and free-ranging white-tailed deer (Hol-
man et al., 1994; Petrini et al., 1995; Holman et al., 2000). Two acute, fatal
cases of babesiosis have been reported in muskoxen in a zoo in Minnesota.
Babesia odocoilei was identified in these animals using DNA-based tech-
niques (Schoelkopf et al., 2005). There are no published reports of Babesia
in Dall’s sheep, mountain goats or moose (Fig. 2.11).

FIGURE 2.12  Arthropoda reported from ungulates of arctic North America, including
Parasites in Ungulates of Arctic North America and Greenland     199

TABLE 2.10  Arthropod parasites in ungulates of arctic North America, including

­Greenland. Data compiled from available published and grey literature

Host and Parasite species Location Herd, region or nearest place name

Caribou or reindeer
Hypoderma tarandi AK, NT, All sampled herds and locationsa–g (Note:
NU latitudinal gradient – reduced prevalence at
higher latitudesc)
YT Porcupineb,e, Chisanae
QC/NL Rivière-George herdb,i
GL Kangerlussuaq-Sisimiutb,j,k; Akia-Maniitsoqb
Cephenemyia trompe AK Western Arcticb,d; Mulchatnad, Northern
Alaska Peninsulad, Nelchinad, Teshepukd;
Various tundral
NT Bathurstb
NU Baffin n, Keewatinl; Bernard Harborl
GL Kangerlussuaq-Sisimiutb,j; Akia-Maniitsoqb
Bovicola sp. NT Bluenose Easto
Solenoptes tarandi AK Anaktuvuk Pass of Brooks Range and Utukok
River south of Barrowa
Chorioptes texanus NT Mackenzie Delta reindeerp
Dermacentor albipictus YT Variousq
NT Woodland caribou North Slavef,q
Linguatula arctica AK Unimak Islandr
NU Baffin Islandn
Dall’s sheep
Bovicola jellisoni AK Kenai Peninsulas
Melophagus ovinus AK Unspecifiedt; Chugach Mtnsd; Alaska Ranged
Dermacentor albipictus YT Variousq
NT Sahtu, South Slave, Deh Chof,q
Hypoderma tarandi AK Seward Peninsulad
NU Victoria Islandg,h
QC Kuujjuaqu
a  Weisser and Kim (1973).
b  CARMA, (2011).
c  Thomas and Kiliaan (1990).

d  K. Beckmen (unpubl. data)

e  S. Kutz, M. Oakley (unpubl. data).

f  B. Elkin (unpubl. obs.).

g  Hughes et al. (2009).

h  Gunn et al. (1991a).

i  Parker (1981).

j  Korsholm and Olesen (1993).

200     Susan J. Kutz et al.

TABLE 2.10  (continued)

k  Clausen et al. (1980).
l  Bennett and Sabrosky (1962).
m  Downes et al. (1985).

n  Ferguson (2003).

o  C. Kashivakura, B. Kenny, G. Verocai, S. Kutz, A. Veitch (unpubl. obs.).

p  Sweatman (1958).

q  Kutz et al., (2009b).

r  Murie (1926).

s  Kim (1977).

t  Bequaert (1942).

u  M. Simard, S. Kutz (unpubl. obs.).

Despite its potential importance as a significant cause of morbidity

and mortality in caribou and muskoxen, there are no published studies
on Babesia in wild caribou or other arctic ungulates in North America.
The ixodid tick, Dermacentor albipictus, is found on moose and wood-
land caribou in the subarctic (Kutz et al., 2009b) but is a one-host tick
and its competence as a vector for Babesia is unknown. Ixodes scapularis,
the known vector of B. odocoilei, is common in white-tailed deer in tem-
perate regions. In Canada, the currently non-contiguous ranges of this
tick are expanding but the northern boundaries of their range are still a
considerable distance from the Subarctic and Arctic (Steiner et al., 2008;
Ogden et  al., 2009). Thus, although white-tailed deer are expanding
their range northwards and may eventually become an important res-
ervoir for B. odocoilei species in the North (Waldrup et al., 1990), it may
be some time before this tick species and Babesia appear in subarctic and
arctic regions.


The known diversity of ectoparasites of arctic ungulates is relatively simple

and includes only one or two representatives in each of the following fami-
lies: the Oestridae (bots), the Linognathidae and Trichodectidae (lice), the
Psoroptidae (mites) and Ixodidae (ticks), and the Lingulatidae (Fig. 2.12,
Table 2.10). In addition, a number of flies, including members of the Mus-
cidae, such as moose flies (Haematobosca alces), members of the Tabanidae
such as horse flies, members of the Hippoboscidae such as the sheep ked
(Melophagus ovinus) (Bequaert, 1942) and members of the Simulidae and
Culicidae (blackflies and mosquitoes, respectively) are reported across
much of the Arctic but are not discussed here. Caribou have the greatest
diversity of ectoparasites whereas muskoxen have the least and appear to
be primarily accidental hosts.
Parasites in Ungulates of Arctic North America and Greenland     201

2.7.1. Diptera Family Oestridae
The Oestridae, nose/throat bots (Cephenemyia trompe) and warbles (Hypo-
derma tarandi) are the most abundant and extensively studied ectoparasites of
arctic ungulates. They are parasites primarily of Rangifer spp. and rarely infest
other ungulate species. They have a Holarctic distribution and are found in
most, but not all, extant Rangifer populations. It is thought that both species
were introduced to west Greenland with reindeer imported from Norway in
1952 (Clausen et al., 1980). Also, the presence of C. trompe on Baffin Island,
NU, appears to be a more recent phenomenon with it first detected on the
southern part of the island in 1997 (Ferguson, 2003). Both species are absent
from translocated reindeer populations in Iceland and South Georgia Island.
Adults of Hypoderma and Cephenemyia are large, robust flies character-
ized by a dense covering of golden and black hairs (Colwell et al., 2006) in
patterns that make them Batesian mimics of several species of bumble bee
(Nilssen et al., 2000; Anderson, 2006). Mimicry of bumblebees presumably
protects the flies from predation by birds (Anderson, 2006). Adults are non-
feeding and must complete all activities using fat reserves built up during
larval development within the host. Females are strong fliers, capable of
flight speeds between 29 and 36km/hr and theoretical flight distances of
up to 330 km (based on flight mill studies) (Nilssen and Anderson, 1995).
First instars are small, translucent white, muscomorph larvae (≈1mm
in length), uniformly covered with small spines (H. tarandi) or slightly
dorso-ventrally flattened and covered with a number of thin spines pri-
marily on the ventral and lateral surfaces (C. trompe). The first instars of H.
tarandi grow to approximately 1cm in length during development beneath
the skin. Second instars are translucent white of up to 1.5cm in length with
widely disbursed short spines on all body surfaces. Third instars are large
(up to 3cm in length) creamy white with all body surfaces having short,
stout, sparsely distributed spines (Colwell et  al. 2006). As third instars
near completion of their development, the cuticle becomes increasingly
melanized and mature third instars are almost completely black.
Third instars that have exited the host bury themselves in the sur-
face litter prior to pupariation. These larvae and the puparia are likely to
encounter freezing temperatures and presumably exhibit cold hardiness
similar to other oestrids (Nilssen, 2006). Development within the pupar-
ium is highly temperature dependent, occurring from 10°C to 35°C with
the maximum development rate at approximately 25°C and not increas-
ing between 25°C and the upper limit (Nilssen, 2006). Overall duration of
the pupal period will range from 7 to 80 days. This exquisite ­temperature
dependence will result in dramatic variation in the timing of adult fly
eclosion between regions and years with differing temperature regimes.
202     Susan J. Kutz et al.

Harassment by oestrid flies can reduce feeding time and lead to

reduced feed intake, reduced summer weight gain, decreased lactation,
reduced calf weights and poorer overall condition that may influence
reproductive success for reindeer (Weladji et al., 2003). The effect of larval
stages on the host, particularly for C. trompe, is less well understood. Cephenemyia trompe

(a) Host and Geographic Ranges. Cephenemyia trompe is found throughout
most of the Holarctic, coincident with the distribution of Rangifer. It is con-
sidered host specific to Rangifer although there are reports of this species
from Odocoileus hemionus in central Ontario, (Bennett and Sabrosky, 1962).
Larvae have been reported from most subspecies of Rangifer (Table 2.10).
(b) Ecology. Cephenemyia trompe are ovoviviparous and females emerge
from the puparia with a compliment of 500–1500 fully developed eggs
(Anderson, 2006). Males aggregate at ecologically characteristic sites, usu-
ally treeless hilltops (Downes et al., 1985; Anderson, 2006) to await pass-
ing females with which to mate. Newly mated females rest for several
days, in order for the larvae to develop within a specialized segment of the
oviduct. When larval development is complete, the females must quickly
search for a suitable host as they do not feed and do not supply nutrient to
their larvae. Individual caribou respond to fly approach by dropping their
head to get their nose as close to the ground as possible which may pre-
vent the accurate deposition of larvae. Harassment by adult Cephenemyia
is thought to induce stress responses similar to those induced by blood-
feeding flies. The fly activity period in southern YT extends from June
through August (Downes et al., 1985). Temperature, wind and cloud cover
are the prime regulators of fly activity with the flies remaining inactive
during cool, windy and inclement weather (Anderson and Nilssen, 1996).
In the YT, males were active at temperatures >6°C (Downes et al., 1985).
Females approach the host from below the head and forcibly eject
small groups of first instars precisely on to the upper lip of reindeer hosts
(Anderson and Nilssen, 1990). Larvae migrate along the roof of the mouth
or tongue to the upper respiratory tract where first instar development
is completed. Second instars move to the pharyngeal region where they
develop within the retropharyngeal recesses or pouches. Third instar
development takes place in the same region and at the completion of this
last stage the larvae are coughed up by the host and expelled. The rate
of larval development may be affected by crowding in the host, where
at high intensities development may not be synchronous (Nilssen and
Haugerud, 1994). This often leads to hosts with all three larval stages
present simultaneously. In general, the second instars are first present in
­mid-January and third instars will be found from early March. Departure
of third instars from the host begins in late April and may continue until
late June (Nilssen and Haugerud, 1994).
Parasites in Ungulates of Arctic North America and Greenland     203

(c) Impacts. Larviposition behaviour alters the normal activity patterns

of caribou (Hagemoen and Reimers, 2002; Anderson, 2006) resulting in
reduced grazing time (Colman et al., 2003) and increased energy expendi-
ture associated with avoidance behaviours. Coupled with the harassment
by Hypoderma tarandi, these flies are a major factor in reduced summer
weight gain, which is crucial to fertility and winter survival, and can have
serious consequences for caribou populations (Hughes et  al., 2009). A
model quantifying weather conditions suitable for fly activity has been
developed (Weladji et al., 2003) and could prove useful for predicting the
impact of these flies on caribou at various localities. The impact of larval
stages of Cephenemyia in caribou is not known. Hypoderma tarandi

(a) Host and Geographic Distributions. Rangifer spp. are the primary hosts for
H. tarandi although there are a few reports of larvae found in muskoxen
in QC and NU and a moose in Sweden (Zumpt, 1965; Gunn et al., 1991a;
Agren and Chirico, 2005; M. Simard, S. Kutz, unpubl. obs.). Host selection
by ovipositing H. tarandi has not been extensively studied, but indications
from other species in the genus suggest that a combination of visual, olfac-
tory and chemosensory evaluations by the fly restrict the host range. For
example, female cattle grubs, H. lineatum, are very selective as to the diam-
eter of hair shaft to which they will attach eggs (Jones, 2000). The ability of
first instars of H. tarandi to penetrate and survive in hosts other than caribou
is likely limited based on the observation that H. lineatum larvae are inca-
pable of penetrating >1–2mm into mouse skin (D. Colwell unpubl. obs.)
and by failure of the same species to either penetrate or survive in goats
under experimental conditions (Colwell and Otranto, 2006). However, ovi-
position and limited larval survival does occur in non-primary hosts, as
exemplified by H. lineatum infestations in bison and horses (Scharff, 1950).
(b) Ecology. Hypoderma tarandi are oviparous and females emerge from
the puparia with a fully developed set of eggs (300–800/ female, Ander-
son, 2006) and are thus ready to mate almost immediately. Males, which
tend to emerge a few days ahead of females, aggregate at ecologically char-
acteristic sites, usually flat graveled areas with sparse plant growth located
along rivers or streams (Anderson, 2006). Mating occurs at these sites and
females depart in search of suitable hosts. Three factors affect oestrid fly
activity with the requirement that ambient temperature be >10°C, wind
or air speed be <6m/s and cloud cover be <40%. These factors have been
used to successfully predict insect harassment (Moerschel, 1999; Weladji
et al., 2003). Females land on the host and thrust their ovipositors into the
pelage, to near the skin surface, where eggs are attached individually to
the hair shaft using ‘glue’ that reduces loss of the eggs. Development of
larvae within the eggs takes place within 7–10 days and larvae migrate
quickly to the skin surface. Larvae penetrate the skin and reside in the
204     Susan J. Kutz et al.

subcutaneous tissues where they become surrounded by a granuloma

referred to as a ‘warble’. Unlike the species that infest cattle, H. tarandi first
instars do not undergo migrations in the connective tissues deep within
the body. The warble provides a nutrient-rich environment where the lar-
vae complete three instars prior to exiting the host. Larval departure from
the host generally begins in early May and is complete by early to mid-July
(Nilssen and Haugerud, 1994; Nilssen, 2006). Larvae that have exited the
host and the puparia are likely to encounter freezing temperatures; they
presumably exhibit cold hardiness similar to other oestrids (Nilssen, 2006).
(b) Impacts. Adult and larval stages may impact the health of cari-
bou. Individual animals respond to oviposition activities by vigorous
leg stamping, presumably to deter or dislodge the flies. This harassment
is thought to induce stress responses similar to those induced by blood-
feeding flies. Additional impact on the host results from the developing
larval stages during winter. The cost to the host results from the energy
cost of development and maintaining the granuloma (warble) surround-
ing the larvae as well as the cost associated with the development and
maintenance of an immune response (e.g. antibody production). Research
on west Greenland caribou suggests that infestation with H. tarandi is a
significant drain on the energy budget of the host and could threaten the
survival of calves and severely reduce fat deposition in pregnant cows
(Cuyler, et  al. 2012) and work on Dolphin-Union caribou, NU, suggests
that increasing warble burdens are negatively associated with the likeli-
hood of pregnancy (Hughes et al., 2009). In other natural systems, it has
been demonstrated that in a situation where food resources are restricted
the larvae can have a major impact on host survival (Milton, 1996). These
observations suggest that, together, adult and larval stages of oestrid flies
may have substantial impact on caribou populations in the Arctic.
Hypoderma tarandi is becoming of increasing concern as a zoonosis
(Lagace-Wiens et  al., 2008); in people, it can cause a serious ophthalmo-
myiasis interna, which often leads to loss of the eye. While the condition
has been reported throughout the range of H. tarandi, there is an increasing
occurrence in the Canadian Arctic. Larvae recovered from affected individ-
uals have been early first instars, but the actual mode of infestation is not
clear. Possible routes include oviposition on the human subjects by errant
flies or accidental transfer of newly hatched larvae from the hide of caribou.

2.7.2. Phthiraptera
Blood-feeding and chewing lice are described from caribou, Dall’s sheep
and mountain goats but not from muskoxen or moose (Durden, 2001).
There is, however, little information available on the specific features of
their biology, epizootiology and impact on their hosts. In addition, there
are few published data on the prevalence and intensity of infestation for
Parasites in Ungulates of Arctic North America and Greenland     205

any of these hosts. The following details on biology are derived from
information on lice affecting domestic livestock (Price and Graham, 1997). Family Linognathidae Solenopotes tarandi

(a) Morphology. Sucking lice are small (usually 1–2mm in length), often blue or
blue–grey in colour, with narrow, pointed heads. They have highly adapted
legs with tarsi modified for grasping hairs on the host’s body. These grasping
‘claws’ help the lice hold their position close to the skin while feeding.
(b) Host and Geographic Distributions. The distribution of S. tarandi is
presumably Holarctic as the original description of this species was from
reindeer in Sweden and it was subsequently identified in barren-ground
caribou in AK (Weisser and Kim, 1973). Solenoptes sp. has not been reported
in moose, muskoxen or Dall’s sheep in the North American Arctic.
(c) Life Cycle. Lice are hemi-metabolous insects with incomplete meta-
morphosis, that is, nymphal stages appear superficially similar to the
adult stages. All life cycle stages are closely associated with their hosts
and they will not survive off the host for long periods. Transmission of
lice occurs by direct contact, although transfer between hosts can occur on
inert objects. Young animals may become infected through transfer from
their dams within a short time after birth.
Both sexes are obligate blood feeders, using small, highly modified
mouthparts that are concealed within the head capsule to obtain numerous
small meals from capillaries in the upper layers of their skin. Data from cattle
feeding species suggest females lay 2–6 eggs per day, which are attached to
the host hair shafts (D. Colwell, unpubl. obs). Eggs complete embryonation
and hatch within 8–11 days of deposition. Lice have three nymphal stages,
which bear a morphological similarity to the sexually mature adult stage.
Each nymphal stage will take 2–4 days to complete. Louse development rate,
at all stages, is highly temperature dependent but is optimal at a narrow tem-
perature range. Temperatures >41°C and 46 °C are lethal for eggs and adults,
respectively, of Linognathus vituli of cattle. Optimal development takes place
between 33 °C and 37 °C. Lice therefore show a seasonal periodicity with
very low numbers in the summer when conditions are hot. Populations begin
to increase as temperatures and solar radiation decline, reaching maximum
levels in late winter. Lice preferentially occupy sites where the host is unable
to groom effectively, but the distribution will become more ­generalized as
the pelage become thicker during fall and winter.
Knowledge on the ecology of S. tarandi from caribou is limited. In one
study, 36 and 74 lice were found exclusively on the head, predominantly
around the ears and cheeks and anterior part of the neck of two of three cari-
bou sampled in AK in June 1971. With the exception of H. tarandi, no other
206     Susan J. Kutz et al.

ectoparasites were recovered from total hide digests of these animals (Weisser
and Kim, 1973). The authors suggested that the predilection for the head
region could be due to the microclimate in this region. Fur on the head is
much shorter than on most of the rest of the body and lacks the dense under-
fur, thus providing a unique temperature and humidity regime that may be
preferred by the lice (Weisser and Kim, 1973). Predilection for the head may
also be a result of the difficulty in individuals grooming that region effectively.
(d) Impacts. Generally, lice do not cause severe problems in large ungu-
late hosts and given the limited literature available it does not appear that
the blood-feeding lice are of serious concern in ungulates in the Arctic.
Rare cases of host disease have been noted in non-arctic ungulates (Foreyt
et al., 1986) where a species of louse has switched host species. Family Trichodectidae Bovicola spp.

(a) Morphology. Chewing lice (Bovicola tarandi, Bovicola jellisoni and Bovic-
ola oreamnidis) are generally small, <2mm in length. These lice are highly
mobile, usually brown or reddish-brown in colour with a characteristi-
cally dorso-ventrally flattened body and broad, rounded head.
(b) Host and Geographic Distributions. Bovicola tarandi are described from
woodland caribou and reindeer, suggesting a Holarctic distribution (Low,

FIGURE 2.13  Dall’s sheep ewe with fur loss. Sheep Mountain, Yukon Territory Canada.
(photograph by S. Kutz, 7 May 2006). (For color version of this figure, the reader is
referred to the web version of this book.)
Parasites in Ungulates of Arctic North America and Greenland     207

1976). Bovicola jellisoni is described as infesting Dall’s sheep (Kim, 1977)

but was originally described from bighorn sheep (Emerson, 1962).
(c) Life Cycle. These lice feed on dead skin cells, hair and oil secretions,
which they abrade from the surface using their chewing mouthparts. There
may be some abrasion of the upper skin layers and there has been demon-
stration that sheep develop antibodies to salivary sections of Bovicola ovis
(James et al., 1998). Sex ratios are highly female biased and parthenogenesis
is a common occurrence in many species (Price and Graham, 1997). Females
deposit less than one egg per day. Embryonation is completed in 7–10 days
producing nymphs, which molt three times before reaching sexual matu-
rity. As with the sucking lice, development is highly regulated by tempera-
ture with a narrow range for optimal development and survival. Chewing
lice can survive off the host for up to two weeks under ideal conditions.
Transmission of lice occurs by direct contact, although phoretic transfer of
chewing lice between hosts by flies occurs occasionally (Mertins et al., 2011).
Bovicola jellisoni was described from two of three Dall’s ewes collected
27 April 1971 from the Kenai Peninsula, AK. One animal had 18 lice, and
the second had approximately 19,300 lice, with 85% of the population dis-
tributed on the sides and belly and 13% around the anus (Kim, 1977). A
high proportion (88%) of the louse population were nymphs, 9% female
adults, and the sex ratio was 3:1 female:male.
(d) Impacts. Chewing louse populations tend to be small on individual
hosts and they have little impact on the host, although there are descrip-
tions of hair loss associated with louse infestation on horses (Larsen et al.,
2005). Occasional reports of hair loss on Dall’s sheep occur (Figure 2.13)
(R. Popko, Mackenzie Mountains, pers. comm.; S. Kutz, Sheep Mountain
Yukon, unpubl. obs.), but aetiology has not been determined. Reports of
skin lesions and hair loss in caribou, with the exception of those associated
with Besnoitia are not common (Kutz, 2007).
There is concern that the potential exists for severe impact on naive
hosts when lice are exchanged between host species that have only
recently come into contact. A severe hair loss syndrome has been described
in black-tailed deer resulting from the transfer of Tricholipeurus parallelus
from white-tailed and mule deer (Bildfell et al., 2004; Foreyt et al., 2004).
On black-tailed deer, the populations of T. parallelus were uncharacter-
istically high and the severity of hair loss lead to death in some cases.
Whether the syndrome was the result solely of the lice or a combination of
factors is not entirely clear, but the consequences for the affected deer were
serious. The problem has become of more concern with the report by Mer-
tins et al. (2011) describing the impact of Bovicola tibialis, a louse brought
to North America with Dama dama (fallow deer), on native species of deer.
It appears that the louse has switched to several native cervids with some
ease and is causing severe hair-loss syndrome in many populations and
is thought to be impacting the well-being of the affected populations. A
208     Susan J. Kutz et al.

potential explanation of the hair-loss syndrome could be the exposure to a

new allergen produced by lice to which the host was not adapted. Pfeffer
et al. (2010) have described an allergen produced by sheep lice (Bovicola
ovis) that is responsible for small reactions seen on the skin of infested
sheep and on non-adapted hosts the reactions could be more severe.

2.7.3. Acari Family Psoroptidae Chorioptes spp.

(a) Morphology. Chorioptes mites are very small, adults being approximately
0.5mm long. The body is oval with legs bearing single stalked pulvilli that
terminate in a cup-like structure.
(b) Host and Geographic Distributions. Chorioptes texanus is considered
to be relatively non-host specific and capable of infesting a wide range of
wild cervids and domestic livestock. It has been reported from reindeer
(Rangifer tarandus) in Canada (Sweatman, 1958), where it was collected
from the ears, but the distribution is likely Holarctic. Chorioptes has not
been reported from moose in North America, but Chorioptes texanus was
reported from moose in Poland (Kadulski, 1996) and a previously unchar-
acterized pathogenic species has been described from the outer ear canals
of moose in Sweden (Hestvik et al., 2007). Chorioptes sp. was observed from
the lower legs of captive muskoxen (B. Wagner, S. Kutz, unpubl. obs.).
(c) Life Cycle. The life cycle comprises five distinct stages, including
egg, larva, protonymph, tritonymph and adult. Based on information
from C. bovis of domestic livestock, the entire life cycle requires from 19 to
28 days to complete on the host (Baker, 1999). Larval and nymph stages
feed on skin debris.
(d) Impacts. In moose, Chorioptes sp. causes significant epidermal and
dermal inflammatory lesions in the outer ear canals (Hestvik et al., 2007).
In captive muskoxen pruritus, mild scaling and hair loss were observed
on the lower legs (S. Kutz, unpubl. obs.). In cattle, an allergic dermatitis
occurs occasionally leading to focal hair loss around the tail-head while in
other domestic animals the predilection site varies (Yeruham et al. 1999). Family Ixodidae Dermacentor albipictus

(a) Morphology. These are medium-sized ticks (3–6mm long) with eyes,
festoons (folds in the posterior margin of the idiosoma), short mouth-
parts and palps with a rectangular basis capitulum. Members of this
Family are characterized by the presence of a dorsal shield, or scu-
Parasites in Ungulates of Arctic North America and Greenland     209

tum, which covers nearly all of the body of males but is confined to the
anterior portion in females and immature stages. The openings of the
respiratory system are associated with near tear-drop-shaped spiracular
plates (also known as stigmal plates) that are characteristic for the spe-
cies (Gregson, 1956).
(b) Host and Geographic Distributions. Dermacentor albipictus is broadly
distributed in temperate North America and is reported from a wide
range of hosts including moose, woodland caribou, mountain goat and
bighorn sheep (Allan, 2001). Recently, D. albipictus appears to be expand-
ing its geographic range north in moose, woodland caribou and elk in
NT and YT, and the potential invasion of barren-ground caribou herds
is a significant concern under current climate warming conditions (Kutz
et al., 2009b).
(c) Life Cycle. Dermacentor albipictus is a one-host tick with all blood-
feeding stages occurring on the same host. Gravid females, once having
mated on the host, drop off in April and March. Oviposition begins in
June. Survival of females, eggs and larvae is reduced by exposure to high
temperatures (Drew and Samuel, 1985). Larvae develop over the course of
the summer and may enter a diapause. Diapause is influenced by photope-
riod (Wright, 1969; Wright, 1971) and larvae are found questing at the tips
of vegetation in September and October (Drew and Samuel, 1985). There
is a high degree of cold tolerance in the larvae allowing persistence during
often hostile periods (Gregson, 1956; Samuel and Welch, 1991). Once on
the host, larvae feed and nymphs can be found within three weeks. This
latter stage does not feed until some time later, often January (Drew and
Samuel 1985). The feeding can take place over a long period, extending
to March, in northern latitudes (Samuel and Barker, 1979). Adult ticks are
found on hosts from March through early June.
(d) Impacts. Feeding by D. albipictus has a range of effects on the host
that may be linked to the host susceptibility, grooming behaviour and
intensity of infection. Moose tend to have the highest burdens, infested
by many thousands of ticks (Samuel and Welch, 1991), caribou and elk
can have moderate infections, and deer tend to support very few ticks
(Welch et al., 1990). The feeding activity of ticks induces an intense itch-
ing that stimulates grooming activity. The grooming can result in dra-
matic hair-loss in some host species such as moose, which can culminate
in adverse effects leading to death. Moose die-offs have been associated
with heavy infestations (Allan, 2001). Other species show only mild alo-
High intensities of infestation of captive reindeer and woodland cari-
bou are associated alopecia, although the confined nature of the animals
may have contributed to the high tick burdens (Welch et al., 1990; Kutz
et al., 2009b). Small numbers of winter tick have also been reported from a
210     Susan J. Kutz et al.

few free-ranging woodland caribou in northern AB and NT (Welch et al.,

1990; Kutz et al., 2009b).

2.7.4. Crustacea, Pentastomida Family: Linguatulidae Linguatula arctica

(a) Morphology. Adult females are large (6–13cm long), dorso-ventrally flat-
tened with numerous pseudo-segments (annuli). In the anterior half, the
annuli are broader than in the caudal half giving the parasites a paddle-
shaped appearance (Riley et  al., 1987; Nikander and Saari, 2006). Males
are smaller (3–4cm long) with a slightly smaller number of annuli. The
number of annuli is a diagnostic feature used to separate L. arctica from
the common species infecting canids L. serrata (Riley et al., 1987).
(b) Host and Geographic Distributions. The sinus worms have been
thought of as primarily parasites of semi-domesticated reindeer in the
Palaearctic; however, there are two reports from North America. It was
reported from a caribou (misidentified as L. serrata, a cosmopolitan par-
asite of carnivores) on Unimak Island, the easternmost Aleutian island
in Alaska (Murie, 1926), and more recently from Baffin Island caribou
(Ferguson, 2003). Based on oral histories from indigenous hunters,
Ferguson (2003) suggests that the sinus worms were present on Baffin
Island prior to the introduction of Norwegian reindeer in 1921. These
reports may suggest a Holarctic distribution for the parasite, but the
apparent discontinuous distribution across the North American Arctic
is enigmatic.
(c) Life Cycle. The reindeer sinus worm has a direct life cycle; an
unusual feature for this group that often utilizes intermediate hosts for
the completion of larval development. Adult sinus worms are found in
the nasal cavity of their hosts where they produce embryonated eggs that
are shed from the host in mucous. The eggs are immediately infective to
grazing calves.
(d) Impacts. Most infections with the sinus worm are found in calves
and animals under two years of age suggesting the development of pro-
tective immunity (Riley et  al. 1987). There has been no reported effect
on infected animals (Haugerud, 1989) despite the presence of significant
pathology in some animals.

2.7.5. Emerging issues and future research for the Arthropoda

With the exception of the Oestridae, the diversity, host and geographic dis-
tribution and impacts of ectoparasites in ungulates of the North American
Arctic are very poorly defined, consisting primarily of a few case reports
Parasites in Ungulates of Arctic North America and Greenland     211

from a few hosts and locations. Caribou appear to have the most and mus-
koxen the least diverse faunas.
The majority of research on host–parasite interactions and on biology
of adult stages has been conducted in the Palaearctic, primarily with the
semi-domesticated reindeer hosts (e.g. C. trompe, H. tarandi and L. arctica).
For the oestrid flies, there is a paucity of data on the biology of the pupal
stages and their response to changes in environment, for example, studies
of the freeze tolerance of mature third instars and pupae are needed. In the
case of H. tarandi, variation in the susceptibility of the various subspecies of
caribou present in North America requires research particularly in light of
the demonstration by Rødven et al. (2009) that the intensity of ­infestation
was higher in lighter coloured individuals (Nørwegian et al., 2009).
The effects of lice and mites on arctic ungulate hosts remain unknown.
Evidence of high infestation intensities (e.g. B. jellisoni in Dall’s sheep),
hair loss of unknown etiologies, and recent recognition of Chorioptes as an
important pathogen in Scandinavian moose suggest that these parasites
may play an important role in host health.
The lifecycles and transmission dynamics of all the ectoparasites
described above are limited or accelerated by ambient climatic conditions,
in particular temperature and relative humidity, but also wind speed
and cloud cover. Defining current faunal diversity, including host and
geographic distributions, together with establishing thermal tolerances,
thresholds and tipping points, are essential steps to understanding the
potential response of these host–parasite systems to ephemeral climatic
events and long-term climate trends.


2.8.1. Parasites alive and well in arctic ungulates

We have defined and reviewed patterns of biodiversity for a complex, suc-
cessful and geographically widespread parasite fauna in caribou, mus-
koxen, Dall’s sheep and moose of the North American Arctic, including
Greenland. At minimum, this fauna consists of 60 described species of
helminths, arthropods and protozoans yet there remains considerable
undescribed biodiversity and probable cryptic species complexes. For the
few parasites that have been studied in some detail, there is strong evi-
dence that they can have significant impacts on individual health and host
population dynamics. Most of these arctic parasites are highly responsive
to climate and climate change and many have important consequences for
the safety, security (sustainability and availability of wildlife populations)
and quality of country foods on which many northern aboriginal peoples
212     Susan J. Kutz et al.

continue to depend. So what have we learned and where do we need to


2.8.2. Parasite biodiversity

It is abundantly clear that, despite the fact that ungulate species are charis-
matic components of northern ecosystems, there remain many basic ques-
tions regarding the biodiversity and faunal structure for their parasites.
Much of the endemic fauna across the high latitudes of the Nearctic was
established through geographic expansion and colonization from Eurasia
under the influence of various biotic and abiotic filters ovet the last 3 mil-
lion years (Hoberg et al., 2012). This historical perspective sets the stage
for understanding the current diversity and also provides a foundation to
explore biological systems under dynamic change. We are now defining
the faunal assembly and patterns of distribution, recognizing that species
richness tends to decrease at high latitudes and on a west to east gradient,
perhaps coinciding with expansion and invasion from Eurasia into North
Recent and ongoing descriptions of new species and cryptic com-
plexes, diagnoses of new genera and definition of new host or geographic
distributions highlight the significant but hidden diversity of helminths
(Hoberg et  al., 1995, 1999; Kutz et  al., 2001d; Hoberg et  al., 2002; Kutz
et al., 2007; Laaksonen et al., 2010b; Haukisalmi et al., 2011; Hoberg et al.,
in press-a,b) and enteric and tissue cyst-forming protozoans (Gudmunds-
dottir and Skirnisson, 2005; Gudmundsdottir and Skirnisson, 2006; Dahl-
gren et al., 2008a; Kutz et al., 2008; Kutz et al., 2009c) in arctic ungulates.
Although diversity for ectoparasites has been explored minimally, hidden
diversity is probable. Ectoparasites may be highly responsive to climatic
changes and also can be important vectors or intermediate hosts for a vari-
ety of pathogens; thus, there is some urgency to understand this fauna
much better in an Arctic undergoing substantial climate change.
Essential to documenting biodiversity are permanent specimen-based
and archival collections that provide historical baselines for contempo-
rary systems and allow comparison across regions and over time (Hoberg
et al., 2003, 2009). Museum archival collections (specimens and associated
informatics) are the critical foundations for documenting change in north-
ern systems (Hoberg, 2010). Importantly, archival collections are ‘self-cor-
recting’ records, that is, specimens can be re-examined and identifications
re-determined as new information and new technology develops. Such
collections have been essential for redescriptions of species, identification
of cryptic species, and correction of historical records (e.g. Hoberg et al.,
1999; Lichtenfels and Pilitt, 1983a). They have also been key resources for
the development of this manuscript where specimens from previously
Parasites in Ungulates of Arctic North America and Greenland     213

published records could be re-examined and reported with the most up to

date taxonomic designations.

2.8.3. Characteristics of arctic parasites – New insights

Parasites of ungulates in the Arctic demonstrate a variety of attributes
that facilitate their persistence in an environment characterized by high
seasonality, extremes of climate and weather (temperature and humidity),
and a generally low abundance and diversity of hosts that varies over
space and time. These factors have operated over both evolutionary and
ecological time, playing critical roles in structuring of the contemporary
parasite fauna (Hoberg, 2012b). Freeze tolerance, arrested development,
overwintering in/on the hosts, large size and high fecundity, long life
spans and defined seasonal characteristics are some of the features that
have ensured the success and often extensive distributions of arctic para-
sites. Freeze tolerance

A key feature of many arctic parasites is their ability to withstand extended
freezing events. Nematodirines and Marshallagia have eggs that are resis-
tant to environmental extremes and subzero temperatures for extended
periods. Both L2 and L3 of O. gruehneri have high overwinter survival on
the arctic tundra. For at least some of the protostrongylids, for example,
U. pallikuukensis and P. odocoilei, both the first-stage larvae in the environ-
ment and developing larvae in gastropod intermediate hosts are able to
overwinter at subzero temperatures; this is predicted also for P. stilesi and
P. andersoni. The cysticerci of T. hydatigena mature within the liver paren-
chyma of arctic ungulates, thus surviving subzero ambient temperatures
longer than more superficial cysticerci that are typical in domestic animals
infected with this cestode. This feature is not described in domestic hosts
and may indicate a behavioural adaptation to subzero temperatures in
sylvatic cycles. At least some species of Eimeria from muskoxen have the
ability to sporulate after extended freezing, an uncommon characteristic
for the Apicomplexans. Freeze tolerance for a number of other parasites
including the tissue forming protozoans (Besnoitia, Toxoplasma, Sarcocystis
and Neospora) and the pupae of Hypoderma and Cephenemyia is unknown
but would certainly be an advantage in the arctic environment. Arrested larval development

Whereas some parasites are able to overwinter in the environment, oth-
ers use a different strategy to survive the extreme cold. Observational
and experimental data demonstrate that arrested larval development is a
dominant feature of the lifecycles for both O. gruehneri and T. boreoarcticus.
214     Susan J. Kutz et al.

Similarly, observational data suggest that Dictyocaulus in muskoxen may

overwinter as fourth-stage larvae in the lungs of calves or yearlings. In
these situations, arrested development over the winter effectively main-
tains the parasites during extended periods of poor environmental condi-
tions and in a hypobiotic state, which conceivably minimizes the energetic
costs to the hosts during periods of possible nutritional stress. Inhibited
development may thus reduce parasite-mediated morbidity and mortal-
ity that would be detrimental to persistence of these directly transmitted
Nematodirus alcidis in moose, however, appears to maintain an arrested
larval population throughout the year and this may serve as a ready reser-
voir to replenish the adult population (Fruetel and Lankester, 1988). Such
a strategy may be particularly important in environments where exposure
to infective larvae is erratic and unpredictable, for example, where host
density is low or climatic conditions are variable. Seasonality
Several arctic parasites display very strict seasonal patterns that coincide
with features of host lifecycles and appear to promote their persistence
in the Arctic. For example, the arrested development of O. gruehneri lim-
its egg production, and subsequent availability of infective larvae, to the
spring and summer, a time when parasites are most likely to develop in
the external environment and be transmitted within migratory caribou
populations. In addition, adult nematodes persist in the abomasa of cari-
bou throughout the winter but are not gravid during this time. Quiescence
of these adult nematodes may minimize the parasite cost to the host at
a time when any eggs produced would not likely survive. Preliminary
­studies on T. boreoarcticus suggest similar patterns. Prepatent periods, fecundity and lifespans

Prepatent periods in arctic helminth parasites differ across taxa and many
appear to be finely tuned to the seasonality of the arctic environment. The
short prepatent period for Taenia krabbei in the definitive host is considered
a potential adaptation to the short summers, where high rates of predation
on ungulate intermediate hosts during the summer would then lead to
egg production throughout the summer (Sweatman and Henshall, 1962).
In contrast, P. cervi, the rumen fluke, and S. tundra, the peritoneal nema-
tode, have very long prepatent periods where infection in one summer
results in peaks in eggs/microfilaria production the following summer
when arthropod intermediate hosts are available and transmission is
most likely to ­succeed.
Several arctic-adapted nematode parasites tend to have long prepatent
periods, are larger in body size and longer lived than their temperate and
Parasites in Ungulates of Arctic North America and Greenland     215

southern relatives. For example, U. pallikuukensis, which appears to have

indeterminate growth (Kutz et  al., 1999), is very large-bodied and long
lived relative to other Muelleriinae lungworms (Hoberg et al., 1995; Kutz
et al., 2001b). Similarly, specimens of T. boreoarcticus are generally consid-
erably larger than those of the closely related T. circumcincta (Hoberg et al.,
1999). Jacobs and Rose (1990) observed large T. circumcincta in domestic
sheep in Greenland and, through experimental studies and cross-infec-
tions, concluded that the large size was more likely a result of environ-

TABLE 2.11  Checklist of parasites confirmed from ungulates of arctic North America,
including Greenland. ‘X’ indicates parasite present in the host in the Arctic and/or

Type of Parasite (reindeer) Dall’s sheep Moose Muskoxen

Nematoda (enteric) (15)

Ostertagia gruehneri X X X
Teladorsagia boreoarcticus X X X
Marshallagia marshalli X X X
Nematodirella sp. X
Nematodirella alcidis X X
Nematodirella longissimespiculata X X
Nematodirella gazelli X
Nematodirus archari/andersoni X
Nematodirus davtiani X
Nematodirus helvetianus X
Nematodirus oiratianus/o. interruptus X
Nematodirus spathiger X
Nematodirus tarandi X X
Skrjabinema tarandi X
Skrjabinema ovis X
Trichuris spp. X X
Trichuris schumakovitschi X
Total species 15 7 10 1 9
Nematoda (tissue)
Dictyocaulus sp. X X
Dictyocaulus eckerti X X
Parelaphostrongylus andersoni X
Parelaphostrongylus odocoilei X X
216     Susan J. Kutz et al.

ment 2.11 
TABLE in the(continued)
host (in particular, low host immunity) rather than a species
Type of Parasite (reindeer) Dall’s sheep Moose Muskoxen
Protostrongylus stilesi X X
Protostrongylus rushi X
Varestrongylus sp. nov. X X X
Umingmakstrongylus pallikuukensis X
Rumenfilaria andersoni X
Setaria sp. X
Setaria yehi X X
Onchocerca cervipedis X X
Total species 10 7 3 6 4
Taenia hydatigena X X X X
Taenia krabbei X X
Taenia arctos X
Echinococcus granulosus X X X
Anoplocephalidae X X X X
Avitellina sp.
Avitellina arctica X
Moniezia sp. X
Moniezia benedeni
Moniezia expansa X
Total species 7 4 2 5 4
Fascioloides magna X X
Paramphistomum sp. X X
Total species 2 2 0 1 1
Protozoa (gastrointestinal)
Giardia sp. X X
Giardia duodenalis assemblage A X
Cryptosporidium sp. X X X
Eimeria sp. X X X
E. ahsata X
E. crandallis X
E. dalli X
E. faurei X
E. granulosa X
E. moshati X
E. ninakohlyakimovae X
E. oomingmakensis X
E. ovina X
Parasites in Ungulates of Arctic North America and Greenland     217

TABLE 2.11  (continued)

Type of Parasite (reindeer) Dall’s sheep Moose Muskoxen
E. parva X
Total species 12 3 6 2 8
Protozoa (tissue) (5)
Besnoitia tarandi X X
Neospora caninum X X X
Sarcocystis spp. X X X X
Toxoplasma gondii X X X X
Trypanosoma sp. X X X
Total species 5 5 3 4 4
Arthropod ectoparasites
Cephenemyia trompe X
Hypoderma tarandi X X
Melophagus ovinus X
Bovicola tarandi X
Bovicola jellisoni X
Solenoptes tarandi X
Chorioptes texanus X
Dermacentor albipictus X X
Linguatula arctica X
Total species 9 7 2 1 1

Total parasite species 60 35 26 18 31

difference from T. circumcincta elsewhere. It is possible that large size may

be a product of both parasite intrinsic characteristics (e.g. genetics) and
host factors. Certainly, reduced host immunity may be an important fac-
tor for arctic ungulates, in particular muskoxen, which appear to be par-
ticularly susceptible to most parasites and parasite-induced disease (e.g.
Alendal and Helle, 1983).
The lifespans of for both O. gruehneri and T. boreoarcticus appear to be
extended, at least two years, an exceptionally long time for this subfamily
of nematodes. Larvae ingested one summer mature the following spring,
produce eggs throughout the summer and persist in the host through the
following winter. Whether they then die or continue to produce eggs the
next summer remains uncertain; however, evidence from experimental
infections suggests that adults of O. gruehneri may survive and produce
eggs for at least two summers. Two reindeer experimentally infected with
a low dose of O. gruehneri and with very minimal opportunity for re-infec-
218     Susan J. Kutz et al.

tion had similar egg counts for two consecutive summer seasons (Hoar
et al., 2012a).
In general, for nematodes, prepatent period is frequently positively
correlated with body size and body size is positively correlated with
egg production (Gemmill et  al., 1999; Rowe et  al., 2008). Large size and
longevity in the Arctic may allow pulses of high egg/larval production
over short seasonal periods but multiple years. Multi-year lifespans may
ensure maintenance of the parasites over years where environmental con-
ditions are inadequate to support development in the environment or
when host densities or behaviour reduce transmission potential. Indeter-
minate growth, large body size and extended fecundity for infections in
highly vagile ungulates are expected to be correlated with a capacity for
invasion and geographic colonization (Hoberg, 2010; Hoberg, in press b). Generalist life history

Another mechanism for survival in the arctic environment may be a
propensity for a generalist life history. The ability to parasitize several
different host species may provide a buffer if one species declines or is
seasonally unavailable. In our study, of 60 parasites that were identified
to the species level, 26 are able to parasitize more than one species of arc-
tic ungulate (Table 2.11). Caribou, however, generally the most abundant
ungulate across the Arctic, may maintain a few more host-specific para-
sites. For example, Besnoitia, Hypoderma, and Cephenemya, are essentially
host specialists. Although they spill-over into muskoxen on occasion, it is
highly unlikely that they could be maintained in this host.

2.8.4. Exploring characteristics of arctic parasites in a broader

Our review has highlighted that differences among arctic ungulate spe-
cies or ecotypes may be very important determinants of parasite com-
munity diversity and transmission patterns. For example, transmission
of parasites among the highly vagile, migratory caribou may differ sub-
stantially from patterns among the highly philopatric Dall’s sheep. Even
within a host species, biodiversity of parasites and patterns of transmis-
sion are likely to differ, for example, between relatively solitary, low-den-
sity and non-migratory Peary and boreal woodland caribou compared
to migratory barren-ground caribou. As our knowledge of the biodiver-
sity and distribution of parasites among these hosts expands, we can
use meta-analyses to explore how host behaviour and ecology influence
parasite distributions within the relatively simple arctic ecosystem. Such
new investigations should include landscape level assessments of genetic
diversity using appropriate fine-scale markers to explore patterns of
Parasites in Ungulates of Arctic North America and Greenland     219

­ istorical and contemporary isolation and expansion for both hosts and
Similarly, we are also at a point where broader comparisons among
parasites of arctic, temperate and tropical systems are needed. In particu-
lar, phylogenetically corrected meta-analyses comparing parasite life-his-
tory patterns and characteristics such as direct versus indirect lifecycles,
arrested development, freeze tolerance, body size, length of prepatent
periods and patency, accumulation of parasites and patterns of age preva-
lence/intensity, host associations and host specialists versus generalists
across broad latitudinal gradients are now becoming possible. Such com-
parisons will provide new insights into host–parasite associations and
adaptations and potential responses to different climatic conditions and
environmental perturbations. Clearly, essential for such meta-analyses is
an understanding of diversity and history for ungulate parasite faunas
both in the Arctic and in temperate and tropical zones.
An exciting area of research that remains virtually unexplored in the
Arctic is the biomass of parasites in the ecosystem and their role in food
webs. Parasites are responsible for a complex array of linkages within the
arctic food web (Kutz, 2012) and understanding how they cycle nutrients
through the environment and the relative importance of this in an arc-
tic ecosystem that is nutrient poor compared to a tropical or temperate
system is an important issue. For example, the biomass of warble larvae
in caribou is substantial. These larvae are composed entirely of nutrients
derived from the caribou host. When they pupate in the environment they
may become important components of the food chain as prey for rodents,
birds and other invertebrates, thus translating caribou biomass into a
potentially wide array of terrestrial vertebrates and invertebrates.

2.8.5. Changing polar environments and host–parasite interactions

Polar environments today are changing at an unprecedented rate in
response to climate change and effects of these changes are now evident in
the biosphere (Callaghan et al., 2004; Post et al., 2009). Accelerated climate
change and extreme weather events are influencing the ecology, impacts
and geographic distribution of endemic parasites in the Arctic (Kutz et al.,
2005; Hoberg, 2010; Laaksonen et al., 2010a) and leading to the expand-
ing ranges and emergence of new parasites at high latitudes (Kutz et al.,
Responses of host–parasite systems to climatic changes will vary and
will be linked to the specific history of faunal assembly, species diversity,
life-history characteristics, and particular tolerances, thresholds and resil-
ience of parasites and hosts (e.g. Kutz et al., 2009b; Hoberg et al., 2008a;
Hoberg et al., 2012). For example, we may expect arthropod transmitted
parasites to respond rapidly, and for the most part positively, to warming
220     Susan J. Kutz et al.

climatic conditions (e.g. Laaksonen et al., 2010a) whereas directly trans-

mitted parasites may be positively or negatively influenced depending
on their thermal tolerances (Kutz et al., 2009b; Hoar et al., 2012b). Addi-
tionally, parasites transmitted by gastropod, and perhaps arthropod,
intermediate hosts may be sheltered from climatic extremes because of
behavioural thermoregulation by these intermediate hosts and therefore
will respond to a warming climate in a more moderated manner (Kutz
et al., 2009b).
Photoperiod at arctic latitudes may be an important factor influencing
the phenology of parasites (Hueffer et al., 2011). While warming climate
may push the potential for more rapid development rates, photoperiod
may temper these responses. For example, the diapause, and consequently
the questing by larvae of the tick D. albipictus, is strongly influenced by
light regime. Under a constant photoperiod of 8h, larvae attached to hosts
at 4 weeks post hatching whereas larvae maintained at 12 and 16 hours
remained in diapause for 10 and 12 weeks, respectively (Wright, 1969,
1971). Thus, photoperiod has a significant impact on larval questing and,
depending on how climate and photoperiod interact, may limit, or accel-
erate, range expansion of this parasite at in the Arctic. Further exploration
of the interaction between climate and photoperiod with respect to para-
site transmission dynamics is important at high latitudes where both these
abiotic features have a very broad range. The breakdown of ecological barriers

Episodic changes in climate and habitat have historically influenced the
assemblage of arctic ungulates and their parasites (Hoberg, in press b).
Ongoing and increasing anthropogenic changes in the Arctic, including
rapid climate warming, landscape perturbation associated with human
activities and animal translocations, can lead to the breakdown of ecologi-
cal barriers that previously may have separated different host species and/
or restricted the movement of parasites either within the North or between
temperate and arctic species (Hoberg, 2010; Hoberg et al., 2012). Such inva-
sions could lead to shifts in parasite communities and parasite transmis-
sion pathways (e.g. through new intermediate/definitive host species
and/or vectors). Given the general pattern for low host specificity among
parasites of arctic ungulates, emergence of new host–parasite interactions
are expected. This is exemplified by muskox translocation and subsequent
expansion leading to sympatry with Dall’s sheep and infection of musk-
oxen with P. stilesi acquired from sheep. With northward range expansion
of southern host and parasite species, disease emergence in naive northern
species and parasite-mediated competition are potential outcomes. Impor-
tantly though, invasion and establishment of new parasites under warm-
ing climatic conditions is not a foregone ­conclusion. For each individual
Parasites in Ungulates of Arctic North America and Greenland     221

parasite species, numerous ecological conditions, including but not limited

to sufficient densities and spatio-temporal distributions of definitive and
intermediate hosts, suitable climate and appropriate thermal tolerances of
the parasite, need to be met before an invasion could succeed.
Other climate-related changes that may influence the parasite fauna, and
subsequently the health and sustainability of wildlife populations, include
increased colonization of northern regions by people and their domestic
animals and thus the potential for rapid invasions by new parasites. Tour-
ism and dumping of ballast water may also influence systems by introduc-
ing new parasites, such as Giardia, which may be transmissible to wildlife. Loss of parasite biodiversity

Another important potential outcome of climate change for parasites in
the Arctic that has received little attention is that of parasite extinctions. As
environmental conditions change and southern species invade, competi-
tion among invasive and endemic parasite species could lead to displace-
ment, extirpation and even extinction of arctic-adapted parasite species.
Similarly, if arctic host species are threatened by extinction, co-extinction
of any host-specific parasites is a reality. Globally, despite the fact that
many host-specialist parasites are anticipated to go extinct with the extinc-
tion of their hosts, there is currently only one parasite listed on the IUCN
red list – the pygmy hog sucking louse (Hematopinidae: Haematopinus oli-
veri) (Whiteman and Parker, 2005). Loss of endemic parasites may reduce
cross-immunity to invasive species and would reduce interspecific com-
petition for invading parasites; thus, it may facilitate establishment of new
parasites. Such losses would also have downstream effects on food webs
as well as consequences for host health. Finally, extirpation of endemic
parasite species would remove a key element of biodiversity and a win-
dow into the evolutionary past of their hosts (Brooks and Hoberg, 2000;
Hoberg et al., 2003, in press b; Whiteman and Parker, 2005).

2.8.6. Directions forward

In the last 15 years, there has been substantial progress in understanding
the biodiversity and ecological interactions of parasites in arctic ungulates
yet there remain significant knowledge gaps. The relative simplicity of the
Arctic makes it extremely enticing to explore host–parasite interactions
much more thoroughly – a perhaps tangible and achievable goal. Climate change

Climate-driven emergence of new parasites and parasite-induced disease
syndromes in the Arctic have heightened our awareness of the sensitiv-
ity of these systems and the value of the Arctic as a model system for
222     Susan J. Kutz et al.

i­ nvestigating the impacts of climate change (Hoberg et  al., 2003; 2008a;
Kutz et al., 2009b). The development of empirical models for the transmis-
sion patterns of protostrongylids has provided predictive tools for antici-
pating potential effects of climate change on distribution and transmission
rates of this group of parasites (Kutz et al., 2005;Jenkins et al., 2006b). Simi-
larly, the determination of a temperature ‘tipping point’ for emergence of
Setaria has provided a measurable climate indicator that can be used to
predict disease outbreaks for this parasite (Laaksonen et al., 2010a). Ini-
tial research on impacts of directly transmitted nematodes suggests that
responses to climate change may differ substantially from those of the
indirectly transmitted protostrongylids and upper temperature thresh-
olds may become important (Kutz et al., 2009b; Hoar et al., 2012b).
An additional consideration is that directional climate change results in
cumulative or incremental processes over a range of time periods (years to
decades) and on regional scales. These processes may interact with extreme
or idiosyncratic (short-term) climatic events, which can influence the emer-
gence of pathogens and disease across landscapes (Hoberg et al., 2008a).
Further modelling of these systems, integrating climate-related impacts on
free-living parasite stages, together with life-history parameters of para-
sites and hosts, is essential for better understanding potential similarities
and differences in the response of these systems to a shifting climate. Parasite ecology

Limiting our understanding of the ecology of parasites in Arctic ungulates
is our incomplete understanding of many of their lifecycles. In some cases,
transmission pathways remain completely unknown and we currently
draw on what is known for related species to infer possible transmis-
sion routes. For example, Besnoitia may have two divergent transmission
routes – through arthropod vectors or through carnivore definitive hosts
– and the response of the host–parasite system to a changing landscape
will differ depending on the transmission route. For other parasites, the
basic transmission cycle may be known; however, the specific develop-
ment and survival parameters, thermal tolerances, thresholds and tipping
points, and alternate, intermediate, and paratenic hosts and vectors are
undescribed. Clearly, knowledge of the transmission route(s), biotic and
abiotic factors influencing the success of these routes and relative contri-
bution of different pathways when they exist is necessary to understand
the drivers of disease and anticipate pathogen impacts under a changing
landscape and different climate scenarios. Impacts
The consequences of parasite infections and the emergence of parasitic dis-
eases for the sustainability of arctic ungulates are still not well ­understood.
Parasites in Ungulates of Arctic North America and Greenland     223

As we look further and in more depth, however, there is increasing evi-

dence to suggest that these changes may be detrimental to individuals
and host populations (Jenkins et al., 2005b; Irvine, 2006; Laaksonen et al.,
2010a). The studies that have provided the most robust information on
impacts on individuals have been those that are longitudinal experimental
studies where parasites have either been removed (i.e. Svalbard reindeer)
or animals have been experimentally exposed (e.g. P. odocoilei). Coupling
these studies with modelling of host population dynamics (e.g. Svalbard)
has provided an insight into potential impacts at the population level.
While experimental manipulations are extremely useful for explor-
ing impacts of parasites on individuals and populations, the frequently
complex logistics and finances have limited the number of such studies
on free-living populations. Also, the components of host–parasite rela-
tionships generating disease are often complex and intricately linked. It
is important to recognize that sometimes the parasites’ adverse effects on
hosts are not obvious and frequently can be very difficult to detect and
quantify. Also, most ungulates are infected with multiple genera and spe-
cies, and synergies among these might be important in generating disease.
In fact, most data on host–parasite systems in arctic ungulates comes
from cross-sectional post-mortem examinations. Despite inherent con-
straints, such studies can be particularly valuable when they are large,
standardized, and repeated on a regular interval to monitor changes over
time and over geographically disparate regions (e.g. Nielsen and Neiland,
1974; Simmons et al., 2001; Kutz et al., 2012). Data from these studies can
provide robust measures of parasite diversity trends, associations with
other biotic and abiotic conditions and host factors (e.g. population size,
trajectory, demographics, sympatric species). They can also help to iden-
tify associations between parasite diversity and abundance and indicators
of host health, age, sex, pregnancy and other physiological parameters.
While it is difficult to irrefutably determine cause and effect, such studies
can lead to important insights and can be used to recognize new ecological
processes and generate new hypotheses. Monitoring programs

Key to successful, monitoring programs are standardized protocols, effi-
cient field techniques, reliable laboratory assays, user-friendly centralized
and comprehensive databases that have adequate and long-term IT sup-
port, and physical archives of whole specimens and specimen DNA (e.g.
Hoberg et al., 2008a). Additionally, it is crucial that any data released be
sufficient to allow meaningful comparisons within and between studies,
for example, date of sampling (to allow for possible seasonal effects), host
age or age class (to allow for age effects), and sample history (to allow for
storage effects such as freezing). For arctic ungulates, the ­Circum­Arctic
224     Susan J. Kutz et al.

Rangifer Monitoring and Assessment network (CARMA) developed such

protocols for Rangifer sampling during International Polar Year (Kutz
et al., 2012). Different levels of field sampling protocols with an increasing
degree of complexity were designed depending on the expertise of the
collector (from lay person through to experienced wildlife disease experts)
and protocols were made publically available on a website. Techniques for
sampling were refined to facilitate scientifically robust and comprehen-
sive sampling. For example, Nobuto filter paper strips were validated for
infectious disease serology and then implemented in the field, thus remov-
ing the need for whole-blood collection and serum separation under field
conditions (Curry 2010; Curry et al., 2011). Application of these protocols
during defined time period across circumpolar Rangifer herds has led to
a much deeper insight into the parasite biodiversity in the Holarctic and
has provided a relatively comprehensive baseline (S. Kutz, J. Ducrocq and
CARMA, 2011, unpubl. obs.). Perhaps limiting the potential future value
of these collections is the absence of a single centralized database that
can manage the data long term, limited capacity of some museums for
archiving specimens and no central repository for archiving of parasite
DNA. The most appropriate collections will involve a large number of
specimens subsampled for both definitive morphospecies identification
and molecular characterization tied to informatics resources for phylog-
eny, ecology and biogeography (Hoberg et al., 2003).

2.8.7. Conclusions
In this review, we have highlighted the current state of knowledge of the
contemporary parasite fauna infecting arctic ungulates of North Amer-
ica and Greenland. Contemporary systems do not exist in an historical
vacuum and understanding the structure of these systems in ecological
time has been, and continues to be, guided by a robust historical founda-
tion. Parasites are key components of arctic ecosystems, bridging trophic
levels and influencing the health and dynamics of wildlife populations.
Although much has been learned, many knowledge gaps remain, related
particularly to parasite faunal structure, the dynamics of the complex
interactions within and among parasite and host communities (includ-
ing invasive fauna) and the population-level impacts on free-ranging
Of equal importance, however, is the very real fact that ungulates play a
key role in the lives of northern aboriginal peoples and changing host–par-
asite dynamics across the North may negatively impact northern residents.
Parasite-mediated population declines could limit availability of arctic ungu-
lates for subsistence or commercial use. Parasitism in individual animals
may be a food safety concern (e.g. Toxoplasma), decrease the quality of the
hides (e.g. warbles) and the meat (e.g. decrease body ­condition and reduce
Parasites in Ungulates of Arctic North America and Greenland     225

amount of highly valued fat), and may make meat aesthetically unpleasing
(e.g. animals with high intensities of Taenia cysts are often discarded) (Kutz
et al., 2009b). In a land where the individual hunter must serve as his/her
own meat inspector, emergence of new disease syndromes can w significant
concerns and uncertainties, resulting in the loss of confidence in country
foods, the loss of cultural traditions, and a reduction in community health.
Arctic ecosystems are undergoing significant perturbations, many of
which have the potential to affect ungulates and other wildlife. Critical
among these is climate warming, which is more marked in the Arctic than
in many other areas of the world. The possible consequences of this warm-
ing for the health and sustainability of the region’s wildlife and people are
difficult to detect, measure and predict. We can take a lesson from the past
across the Arctic, a region strongly influenced by episodic shifts in climate
and where host–parasite systems have diversified under cycles of dynamic
and rapid change. Invasions, accompanied by geographic and host colo-
nization have shaped the structure of diversity that we have documented.
We anticipate that such processes will continue to have a substantial influ-
ence on high latitude systems. Further, it is possible that some effects of
new climate regimes might be mediated through parasites, for many of
which host and geographic distributions, transmission, abundance and
health impacts depend on local and regional environmental conditions.

Numerous people have contributed to this manuscript. Thanks go the CARMA network, in
particular the wildlife disease experts, wildlife biologists and managers, and the community
members who have collaborated on much of the work presented in this manuscript; Dean
Brown, Sylvia Checkley, Patricia Curry, Nathan deBruyn, Maëlle Gouix, Jesse Invik, Cyntia
Kashivakura, Lynn Klassen, Alessandro Massolo, Karin Orsel, Karin Seeger, Rene Span, Jillian
Steele, Jian Wang, Brent Wagner, Jessica Wu, Jayninn Yue and many others who contributed
to scientific discussions, sample processing and the smooth operations of the Kutz labora-
tory at the University of Calgary Faculty of Veterinary Medicine, and at the Western College
of Veterinary Medicine, University of Saskatchewan; Mathieu Dumond, Luigi Torretti and
Jorgan Bolt (Government of Nunavut); Alasdair Veitch, Richard Popko, Marsha Branigan,
Jan Adamczewski and John Nagy (Government of the NT); Philip Merchant, Michelle Oak-
ley, Rick Farnell, Rick Ward (Yukon Government), and Manon Simard (Nunavik Research
Centre, Quebec) who have contributed many samples and dynamic discussions over the
years; Nathan Pamperin, Jeff Wells and many others with the Alaska Department of Fish and
Game who contributed information and images for this work. We also thank Patricia Pilitt
and Arthur Abrams, Associate Curators at the US National Parasite Collection, ARS, USDA
Beltsville for their contributions to the morphological and molecular characterization of vari-
ous nematode parasites from northern ungulates over the past decade.
Grants to S. Kutz and associated laboratory members contributed to the work that is
presented in this manuscript: NSERC Discovery, NSERC Northern Supplement, NSERC Spe-
cial Opportunities grants; Environment Canada International Polar Year funding; Alberta
Innovates; University of Calgary; Sahtu Renewable Resources Board; Cumulative Impacts
226     Susan J. Kutz et al.

­ onitoring Program, NWT; Alberta Conservation Association – Grants in Biodiversity; W.

Garfield Weston/Wildlife Conservation Society; Northern Scientific Training Program; Arctic
Institute of North America Grant in Aid and Nassivik Centre for Inuit Health. Further, and in
part, this is a contribution of the Beringian Coevolution Project a multi-national research collab-
oration to explore diversity across the roof of the world supported by grants from the National
Science Foundation (DEB 0196095 and 0415668) to J.A. Cook at the Museum of Southwestern
Biology, University of New Mexico and to E.P. Hoberg at the US National Parasite Collection.

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Neorickettsial Endosymbionts
of the Digenea: Diversity,
Transmission and Distribution
Jefferson A. Vaughan, Vasyl V. Tkach
and Stephen E. Greiman

Contents 3.1. Introduction 254

3.2. Taxonomy and Phylogeny of Neorickettsia 256
3.2.1. Systematic position of Neorickettsia 256
3.2.2. Taxonomy and phylogenetic interrelationships
among species of Neorickettsia 258
3.3. Ecology and Transmission of Neorickettsiae 260
3.3.1. Neorickettsia helminthoeca and SPD 261
3.3.2. EFF agent 265
3.3.3. Neorickettsia sennetsu and Sennetsu fever 267
3.3.4. Neorickettsia risticii and PHF 270
3.3.5. SF agent 275
3.3.6. Rainbow trout agent 275
3.3.7. Neorickettsia sp. from needlefish in Cambodia 276
3.3.8. Catfish agents 276
3.4. Geographic distribution of Neorickettsia 277
3.5. Phylogenetic associations between
Neorickettsia and Digenea 283
3.6. Advances in genomics and molecular biology
of Neorickettsia 285
3.7. Gaps in current knowledge and future perspectives 287
Acknowledgements 289
References 289

Department of Biology, University of North Dakota, Grand Forks, ND, USA

Advances in Parasitology, Volume 79 © 2012 Elsevier Ltd.

ISSN 0091-679X, All rights reserved.

254     Jefferson A. Vaughan et al.

Abstract Digeneans are endoparasitic flatworms with complex life ­cycles

and distinct life stages that parasitize different host species.
Some digenean species harbour bacterial endosymbionts known
as ­Neorickettsia (Order Rickettsiales, Family Anaplasmataceae).
­Neorickettsia occur in all life stages and are maintained by verti-
cal transmission. Far from benign however, Neorickettsia may also
be transmitted horizontally by digenean parasites to their verte-
brate definitive hosts. Once inside, Neorickettsia can infect macro-
phages and other cell types. In some vertebrate species (e.g. dogs,
horses and humans), neorickettsial infections cause severe disease.
Taken from a mostly parasitological perspective, this article sum-
marizes our current knowledge on the transmission ecology of
neorickettsiae, both for pathogenic species and for neorickettsiae
of unknown pathogenicity. In addition, we discuss the diversity,
phylogeny and geographical distribution of neorickettsiae, as well
as their possible evolutionary associations with various groups of
digeneans. Our understanding of neorickettsiae is at an early stage
and there are undoubtedly many more neorickettsial endosymbi-
oses with digeneans waiting to be discovered. Because neorickett-
siae can infect vertebrates, it is particularly important to examine
digenean species that regularly infect humans. Rapid advances in
molecular tools and their application towards bacterial identifica-
tion bode well for our future progress in understanding the biology
of Neorickettsia.


Today, biologists, healthcare professionals and veterinarians are well

aware that blood-sucking arthropods can serve as biological vectors of
disease. Fewer realize that endoparasitic helminths can also act as vec-
tors of animal and human infectious diseases. However, examples of this
have been known for a long time. Three of the earliest known examples
include turkey blackhead disease caused by a flagellated protist Histomo-
nas meleagridis transmitted, among other ways, by a nematode Heterakis
gallinarum (Graybill and Smith, 1920; Tyzzer, 1934; Ruff et al., 1970); swine
influenza caused by a virus that can also be transmitted by a parasitic
nematode, Metastrongylus apri (Lee, 1971; Shope, 1941, 1943), and salmon
poisoning disease (SPD) caused by a bacterium transmitted by a digenean
­Nanophyetus salmincola (Lee, 1971; Philip, 1955).
Transmission of bacterial diseases by digenean parasites was almost
simultaneously and independently discovered on the opposite sides of
the globe during the mid-1950s. In North America, Philip et  al. (1953,
1955) found that a lethal dog disease previously well known as ‘salmon
dog poisoning’ is caused by a rickettsial agent transmitted by an intestinal
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     255

fluke N. salmincola. Meanwhile, Japanese researchers (Fukuda et al., 1954;

Misao and Kobayashi, 1954) discovered that a previously known disease
of unknown aetiology, the Sennetsu fever, is also caused by a new rickett-
sial agent associated with flukes. Philip et al. (1953) erected a new genus,
Neorickettsia, for this new bacterium species.
The genus Neorickettsia (Family: Anaplasmataceae) comprises a small
group of obligate intracellular bacteria normally endosymbiotic within
digeneans. Digenean life cycles are complex and typically involve several
stages parasitizing different host species. Neorickettsiae persist within all
stages of the fluke and thus are maintained through vertical transmission.
Under certain circumstances, adult flukes may pass their neorickettsial
endosymbionts to the vertebrate definitive hosts. Once inside, neorickett-
siae invade and multiply within the cells of the vertebrate. In some ver-
tebrates, neorickettsial infections of macrophages, monocytes and other
cells types lead to severe, sometimes fatal, disease. Currently, there are at
least seven species/genotypes of Neorickettsia and four distinct diseases
attributed to Neorickettsia.
With a few exceptions, studies of Neorickettsia have been traditionally
carried out by bacteriologists, medical and veterinary researchers, while
helminthologists have rarely participated in these research endeavours.
Despite the in-depth research published on different aspects of molecu-
lar biology, immunology, diagnostics and treatment of neorickettsiae and
neorickettsial diseases, the quantitative aspects of transmission of these
bacteria and their ecological and evolutionary interrelationships with
their invertebrate and vertebrate hosts have received much less attention.
Neorickettsia transmission systems are inextricably intertwined with com-
plex multihost life cycles of digeneans. Thus, full elucidation of the trans-
mission patterns of these neglected, but potentially widespread diseases
will require equal participation of helminthologists, rickettsiologists, epi-
demiologists and vector biologists.
Recent progress in molecular techniques, particularly the polymerase
chain reaction (PCR) and DNA sequencing, has made possible the efficient
and reliable detection of Neorickettsia at every step of their circulation,
whether in the digenean host of the neorickettsiae or in the invertebrate
and vertebrate hosts of the digenean. The same technology also allows
for reliable identification of the digeneans, regardless of the stage of their
development. Increasing number of Neorickettsia DNA sequences in the
GenBank and other internationally accessible public databases have facili-
tated rapid comparisons of genotypes discovered in different parts of the
world. Phylogenetic reconstructions of Neorickettsia have revealed new
lineages, in some cases potentially new species. Recent publication of
complete genomes of two Neorickettsia species opens new possibilities for
studies of their evolution and phylogeny, metabolism and treatment of
diseases caused by these bacteria.
256     Jefferson A. Vaughan et al.

Several significant reviews have been published on different aspects

of Neorickettsia and neorickettsial diseases. These reviews usually covered
Neorickettsia as a part of a larger discussion of diseases caused by various
groups within the Anaplasmataceae (Rikihisa, 1991, 2003, 2010; Walker
and Dumler, 1996; Rikihisa et al., 2005) or focused on particular species
of Neorickettsia of veterinary importance (Mulville, 1991; Palmer, 1993;
­Madigan and Pusterla, 2000; Headley et al., 2011).
This article primarily focuses on the current knowledge of the trans-
mission ecology, diversity, phylogeny and distribution of neorickettsiae.
We are not covering pathology and therapy, diagnostics and immunology
of neorickettsial diseases nor do we review recent advances in biochemis-
try and molecular biology (comparative genomics and proteomics) to any
significant extent. Readers primarily interested in these topics may refer to
the reviews mentioned above or other relevant publications (e.g. Cordes
et al., 1986; Brouqui and Raoult, 1990; Barnewall et al., 1999; Zhang et al.,
1997, 1998; Rikihisa, 2003; Rikihisa et  al., 2004; Hotopp et  al., 2006; Lin
et al., 2009; Gibson et al., 2010, 2011).


3.2.1. Systematic position of Neorickettsia

The classification of rickettsiae and other intracellular bacteria was tra-
ditionally based on biological, morphological or immunological charac-
teristics. Introduction of DNA sequencing has dramatically changed the
field. Among other findings, molecular phylogenies have led to a reor-
ganization of the order Rickettsiales into two families, Rickettsiaceae
and Anaplasmataceae (Dumler et  al., 2001). This revision was based
primarily on phylogenetic analyses of 16S ribosomal RNA (rRNA) and
groESL gene sequences. Secondary characters included outer membrane
protein sequences (amino acid or gene sequences) and biological char-
acteristics such as morphology, host cell tropism, disease ecology and
clinical presentation. Neorickettsia is one of the four generally accepted
genera belonging to the family Anaplasmataceae, namely Anaplasma,
Ehrlichia, Wolbachia and Neorickettsia (Dumler et  al., 2001; Taillardat-
Bisch et  al., 2003; Rikihisa, 2010; Fig. 3.1). Recent publications (Seng
et al., 2009; Rikihisa, 2010) suggest the existence of three to five addi-
tional genera in the family (Fig. 3.2), some of which are not formally
described yet.
All Anaplasmataceae are obligate intracellular bacteria that grow
within membrane-bound vacuoles of host cell origin (=morulae). The gen-
era Anaplasma and Ehrlichia are exclusively tick borne and include species
of medical or veterinary importance. Aegyptianella is also considered by
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     257

FIGURE 3.1  Phylogenetic interrelationships among the Anaplasmataceae based on

Bayesian analysis of partial 16S rRNA sequences. (For color version of this figure, the
reader is referred to the web version of this book.)

some as another valid genus of the Anaplasmataceae (e.g. Rikihisa, 2010),

although in our analysis based on partial ribosomal 16S sequences, Aegyp-
tianella clustered together with members of Anaplasma (Fig. 3.1). Both
are transmitted horizontally from tick to vertebrate to tick and vertical
transmission plays little role in their natural cycle. The genus Wolbachia
infects the ovaries of many species of arthropods and filariid nematodes
and is transmitted exclusively through vertical transmission. There are no
known vertebrate hosts of Wolbachia.
The most genetically divergent genus is Neorickettsia with all species
apparently endosymbiotic in digenean flukes. Neorickettsia are unique
among the Anaplasmataceae in that both vertical transmission and hori-
zontal transmission (at least from fluke to vertebrate) have been docu-
mented (Cordy and Gorham, 1950; Gibson et al., 2005). Neorickettsia can be
grown in vitro within certain cell types (e.g. macrophages and monocytes)
of various ­vertebrate species (e.g. mouse, dog and human).
258     Jefferson A. Vaughan et al.

FIGURE 3.2  Phylogenetic position of the new genotypes of Neorickettsia and two
­putative new genera of Anaplasmataceae found by Seng et al. (2009) in the tract of fish
in Southeast Asia (adapted after Seng et al., 2009, with permission).

3.2.2. Taxonomy and phylogenetic interrelationships among

species of Neorickettsia
Presently, there are three published named species and four genotypes
of Neorickettsia, four of which cause distinct diseases, including a human
disease (Table 3.1). In addition, we have recently identified two more
genotypes from digeneans parasitic in North American catfishes (V.V.
Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data; Fig. 3.3).
The separation between species in literature is based primarily on levels
of 16S rRNA sequence divergence (Dumler et  al., 2001; Stackebrandt
et  al., 2002). Biological differences among the neorickettsial species
are borne out by the fact that different species produce clinical illness
within certain vertebrate species but not in others. At the same time,
different species demonstrate antigenic relatedness, as evidenced by
immunological cross-protection conferred between different neorickett-
sial species. For example, N. sennetsu causes clinical illness in humans
but not horses. However, when horses are inoculated with N. sennetsu,
they become immune against challenge with N. risticii, a species nor-
mally pathogenic to horses (Rikihisa and Jiang, 1988).
Currently, the taxonomy and principles of species differentiation
among Neorickettsia species are far from being stable and universally
agreed upon. For instance, multiple neorickettsial infections in digene-
ans from Korea identified as N. risticii (Chae et al., 2003; Park et al., 2003)
TABLE 3.1  Neorickettsia species/genotypes described in literature and diseases caused by them

Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution    

Neorickettsia Vertebrates Neorickettsia Vertebrate cell type
species/genotypes Disease affected by disease localization infected Geographic distribution First described

Neorickettsia Sennetsu Humans, rodents Lymph nodes Monocytes, Japan, Malaysia, Laos, Fukuda et al.
sennetsu fever (exp.) endothelium Thailand (1954)
SF agent Not known Mice (exp.), dogs Not known Macrophages Japan Fukuda et al.
(exp.) (1973)
Neorickettsia Salmon Canids Lymph nodes Macrophages North America (Pacific Philip et al.
helminthoeca poisoning slope of Cascade (1953)
Mountains), Brazil
EEF agent Elokomin Bears, dogs (exp.) Lymph nodes Macrophages Northwestern USA Farrell et al.
fluke fever (1973)
Neorickettsia Potomac Horses Large colon Glandular epithelia, USA, Brazil and South Holland et al.
risticii horse fever macrophages, Korea (1985c)
Rainbow trout Not known Not known Not known Not known USA – northern Cali- Pusterla et al.
agent fornia (2000)
Neorickettsia sp. Not known Not known Intestine Not known Cambodia Seng et al.
from needlefish (2009)

260     Jefferson A. Vaughan et al.

FIGURE 3.3  Phylogenetic tree of currently known species and genotypes of Neorickettsia
resulting from Bayesian analysis of partial 16S rRNA sequences.

may not belong to this species. Based on the levels of sequence homology
of 16S gene provided by these authors, their isolates are more closely
related to the ‘rainbow trout’ genotype of Neorickettsia reported from
North America and, thus, may belong to a phylogenetic lineage different
from that of N. risticii. Although Chae et al. (2003) did not present a phy-
logenetic tree and did not submit sequences to a publicly accessible data-
base, their work demonstrate the potential of finding additional forms
in eastern and southeastern Asia. Our preliminary sampling and screen-
ing of a variety of digenean taxa from North America (V.V. Tkach, J.A.
Schroeder and J.A. Vaughan, unpublished data; Fig. 3.3) demonstrate
that novel lineages of Neorickettsia may exist in other parts of the world
as well.


There are four distinct diseases described in the medical/veterinary lit-

erature attributable to Neorickettsia; SPD, Elokomin fluke fever (EFF),
Sennetsu fever and Potomac horse fever (PHF; Table 3.1). The causative
agents for these diseases are generally regarded as separate species based
on differing pathologies, serology, antigenic profiles and DNA sequence
analyses. In addition, there are at least five other species/genotypes of
neorickettsial endosymbionts whose pathogenicity to humans or other
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     261

vertebrates is not known. The discovery of non-pathogenic Neorickettsia

genotypes resulted largely from ecological studies targeting the patho-
genic species. For example, studies on sennetsu fever discovered the SF
(abbreviated from Stellantchasmus falcatus) agent and ecological studies on
N. risticii discovered the neorickettsiae provisionally designated as rain-
bow trout agent, catfish agent 1, catfish agent 2 and undefined N. risticii-
like agents.

3.3.1. Neorickettsia helminthoeca and SPD

It was common knowledge among native Americans and white settlers
along the Pacific coast of northern California, Oregon and Washing-
ton that if dogs were allowed to eat the dead or dying ‘spawned out’
salmon, the dogs were likely to become very ill and die. It was assumed
that the fish contained a toxin that was somehow poisonous to dogs,
foxes and coyotes – but not to other fish-eating carnivores such as rac-
coons or mink. Thus, the affliction got its name ‘salmon poisoning of dogs’.
Symptoms include rapid onset of fever and weight loss, accompanied
later by vomiting and black, bloody diarrhoea. If left untreated, death is
almost certain (90% mortality rate) within 2 weeks after onset. Because
of the extreme severity of this disease, concern about SPD among vet-
erinarians and dog owners in the Pacific Northwest persists to the pres-
ent day.
As early as in 1911, Pernot (1911) demonstrated that SPD was not due
to a toxin but instead was caused by an infectious agent. Blood from sick
dogs was injected into healthy dogs. After an incubation period of 2–4 days,
injected dogs developed symptoms characteristic of salmon poisoning.
Serial injections of blood from these dogs into naive dogs also produced
disease with similar symptoms and incubation periods. Furthermore,
the few dogs that managed to survive their illnesses were immune to the
effects of subsequent injections. However, the exact aetiology of the infec-
tion remained unknown until Donham (1925) made a key observation. He
reported that autopsied dogs that died of SPD all harboured minute adult
digenean flukes (later identified as N. salmincola by Chapin, 1926). Don-
ham correctly surmised that the afflicted dogs had acquired their adult
flukes by ingesting fluke cysts (=metacercariae) found in the flesh and
internal organs of local salmonid fish. Furthermore, he speculated that
presence of the fluke was a necessary component of contracting the dis-
ease. Simms et al. (1931a, b, 1932) demonstrated conclusively that metacer-
cariae and adult flukes of locally collected N. salmincola caused SPD when
fed or injected into dogs. They suspected that the infection was rickettsial
or haemosporidian in origin. Their hypothesis was confirmed when Cordy
and Gorham (1950) described intracytoplasmic ­rickettsial-like organisms
in reticuloendothelial cells from Giemsa-stained lymph node impression
262     Jefferson A. Vaughan et al.

smears taken from a dog that died of salmon poisoning. Philip et al. (1953)
named the agent N. helminthoeca in recognition that it was a new type of
rickettsia and that digeneans were essential to their transmission.
During the 1950s and 1960s, two main groups of researchers studied
the disease. Researchers at Oregon State University (Millemann et  al.,
1964; Millemann and Knapp, 1970; Gebhardt et al., 1966; Baldwin et al.,
1967; Nyberg et al., 1967 Schlegel et al., 1968) conducted ecological stud-
ies on the digenean parasite and its intermediate and definitive hosts. At
the National Institutes of Health Rocky Mountain Laboratory in Hamilton
MT, C.B. Philip and his colleagues performed studies on the transmis-
sion and pathology of the aetiology agent (Philip at al., 1954a, b; Philip,
1955). From the work of these and others, it is now known that the disease
agent, N. helminthoeca, is found in all life stages of the digenean parasite,
N. ­salmincola (Fig. 3.4 for fluke life cycle; Bennington and Pratt, 1960).

FIGURE 3.4  Circulation of Neorickettsia helminthoeca (white dots) through life cycle
of its digenean host, Nanophyetus salmincola. Images by T. Dieter (snail) and T. Saxby
(trout), Integration and Application Network, University of Maryland Center for Environ-
mental Science ( Images of raccoon and dog are from the
clipart library sold with CorelDraw X4 software package. (For color version of this figure,
the reader is referred to the web version of this book.)
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     263

In nature, dogs acquire infections by consuming fish containing N. sal-

mincola-infected metacercariae. When dogs eat infected fish, the ingested
fluke metacercariae mature to adults deep within the mucosa of the upper
portion of the small intestine. Adult worms begin producing eggs in 5–10
days, which corresponds closely to the normal prepatent period of SPD
symptoms in dogs. The mechanism by which neorickettsial organisms are
transferred from the developing fluke to intestinal tissues and into macro-
phages of the dog is unknown. If left untreated, most dogs die within 6–10
days after onset of clinical symptoms. During the rapid course of disease,
gross pathology is largely restricted to the visceral lymph nodes, which
present as enlarged and fleshy, often with areas of haemorrhage and necro-
sis. The relatively mild pathology induced by SPD belies its severe and
lethal consequences, suggesting that N. helminthoeca possesses a highly
potent virulence factor(s) (Philip et al. 1954a). Yet, experimental infections
with SPD fail to produce more than a transient fever in other non-canid
mammals, including raccoons, bears, mink, bobcats, domestic cats, guinea
pigs, rats, mice or hamsters (Cordy and Gorham 1950, Simms et al. 1931b;
Simms et al., 1932). Humans can be infected with the fluke (Eastburn et al.
1987; Harrell and Deardorff 1990) but are apparently refractory to the dis-
ease. Philip (1955) infected himself by eating raw metacercarial-infected
trout, samples of which produced a fatal infection when fed to a dog. He
suffered no ill effects, but some parasites did attain maturity as evidenced
by the appearance of a few eggs in his stool 10 days after ingestion of the
raw fish.
Indeed, because of the unique pathogenicity of SPD against canids,
wildlife biologists have investigated the feasibility of using fish from SPD-
endemic regions as a possible alternative to traditional poisoned baits to
control coyotes, Canis latrans (Foreyt and Thorson, 1982, Foreyt et al., 1987;
Green et al., 1986; Foreyt and Gorham, 1988). Dogs, foxes and coyotes that
recover from SPD, either naturally or via antibiotic therapy, are immune
to subsequent infection (Simms et al. 1931a). However, the flukes in their
intestines continue to harbour infectious neorickettsiae and convalescent
dogs may continue to shed neorickettsia-infected fluke eggs in their faeces
(Philip et al 1954b).
In the laboratory, SPD has been transmitted experimentally from dog
to dog by intra-peritoneal injection of blood or lymph node homogenates
prepared from sick dogs (pre-patent period = 2–4 days; Philip et al. 1954b).
During experiments to determine if SPD could be transmitted among
dogs by direct contact, Bosman et al. (1970) successfully infected dogs via
aerosolization and enemas of lymph node suspensions and rectal mucosa
homogenates. This indicated that in theory, SPD could be communicable.
However, contagious infection within a natural setting is probably rare
because Sims (1932) reported that over the course of 7 years, over 100
susceptible dogs were maintained in kennels together with dogs infected
264     Jefferson A. Vaughan et al.

with SPD and in no instance was SPD transmitted to susceptible dogs by

such contact. This is in spite of the fact that SPD-stricken dogs produce
vomit and diarrhoea.
SPD has also been transmitted experimentally from fluke to dog by
intra-peritoneal injection of whole and macerated adult flukes (pre-patent
period = 6–7 days) and of snail tissue containing rediae (pre-patent period
of 28–33 days; Philip et al. 1954a). The disease was also successfully trans-
mitted by injecting dogs with fluke eggs homogenized in glass tissue
grinder – but not with intact eggs – indicating that infectious neorickett-
siae are contained within the interior of the unembryonated N. salmincola
eggs but not on the exterior surfaces of the egg shells (Nyberg et al. 1967).
This was conclusive proof that N. helminthoeca is transmitted transovari-
ally to successive generations of digeneans.
Until recently, SPD was considered to be restricted exclusively to west-
ern United States and Canada, ranging from the Pacific coast westward
to the Cascade Mountains and longitudinally from southern Vancouver
Island (Booth et  al. 1984) to the Sacramento River of northwest Califor-
nia (Sykes et al. 2010). However, N. helminthoeca has also been confirmed
recently in south-central Brazil using immunological and molecular tech-
niques (Headley et al 2004, 2009). This indicates that there is an alternative
life cycle for SPD and that it is more widespread than previously appreci-
ated. The fluke species responsible for SPD transmission in Brazil remains
unknown. In North America, SPD is only transmitted by N. salmincola.
Thus, the geographic distribution of SPD is constrained by the distribu-
tion of N. salmincola that is in turn determined solely by the distribution
of the fluke’s first intermediate host, Juga silicula (Family: Pleuroceridae).
This snail species (sometimes referred to as Oxytrema silicula) is common
in streams and rivers of the Pacific Northwest but is found nowhere else
(Bennington and Pratt 1960). Although J. silicula serves as a host to several
other digenean species (including Acanthatrium oregonense, which har-
bours a different Neorickettsia species – see N. risticii below), the asexual
development and production of cercariae by N. salmincola can only occur
in this snail species (Millemann and Knapp 1970).
Juga silicula snails become infected after N. salmincola eggs hatch and
miracidium penetrates the snail. Over several months, digenean rediae
within the snail undergo numerous asexual generations and eventually
produce thousands of stub-tailed xiphidiocercariae, which are shed into
the surrounding water. Presumably, the neorickettsiae proliferate in tan-
dem with their larval digenean hosts within the snail. Upon contact with
salmonid fish, the xiphidiocercariae of N. salmincola rapidly penetrate
the skin and move into muscle and viscera of the fish where they encyst
and enter the metacercaria stage. Salmon generally acquire N. salmincola
metacercarial parasites during their years as young fish in freshwater.
Neorickettsiae within N. salmincola metacercariae have been shown to remain
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     265

viable for at least 3 years during the oceanic phase of the salmon life cycle
(Farrell et  al. 1964). Thus, dogs can acquire SPD by eating fingerlings,
smolts or ocean-caught adult fish (Millemann et  al. 1964). Cooking or
freezing (–20°C, 24h) the fish kills both the parasite and the neorickettsial
endosymbiont, although SPD has been reportedly transmitted through
smoked (kippered) salmon (Farrell et al. 1968, 1974). Nanophyetus salmin-
cola metacercariae have been found naturally infecting other types of fish
besides salmonids (e.g. shiner, sculpin and lamprey) and N. salmincola
cercariae have been demonstrated experimentally to penetrate and form
metacercariae in even more fish species and even a salamander (Gebhardt
et al., 1966). Thus, the potential for canids to contract SPD goes beyond
just eating raw salmon or trout.
Adult N. salmincola flukes have been found to occur naturally in the
intestines of 12 species of mammals and 3 species of piscivorous birds in
western Oregon, USA (Schlegel et  al. 1968). However, parasite loads in
many of the species were low. Raccoons and spotted skunks were con-
sidered to be the principal definitive hosts of N. salmincola based on their
abundance, their propensity to eat fish and defecate in or near the water
and the high prevalence (100% and 75%, respectively) and intensities of
fluke infections (average of 57,571 and 2613 flukes per animal, respec-
tively) in these species. Although raccoons do not become clinically ill
with SPD, Philip (1955) reported that a suspension of ca. 500 adult N.
salmincola flukes taken from a raccoon at necropsy caused a characteris-
tic fatal infection of SPD when injected into a dog. Thus, neorickettsial
endosymbionts retain their viability within adult flukes, regardless of
whether the fluke parasitizes a neorickettsia-susceptible canid or a neor-
ickettsial-refractory non-canid host. This indicates that raccoons and pos-
sibly many other vertebrate species, contribute to the natural cycling of N.
helminthoeca, and dogs, although victims of disease, are not required for
maintenance of the neorickettsiae.
Interestingly, a close relative of N. salmincola, namely N. schikhobalowi,
infects fish-eating mammals, including humans, living alongside the
Amur and Ussuri Rivers of southeastern Siberia. The ecology of the fluke
is similar to its sister species in the Pacific Northwest, yet SPD is not
known in the region and the local dogs eat raw fish and carry adult flukes
in their intestines (Filimonova, 1963). This suggests that Asian species of
the Nanophyetus fluke do not harbour neorickettsiae or if they do, they
harbour a different species of Neorickettsia that is non-pathogenic to dogs.

3.3.2. EFF agent

In 1973, Farrell and colleagues published a series of papers describing what
they designated as a second neorickettsial agent transmitted by the same
fluke vector, N. salmincola (Farrell et  al., 1973; Sakawa et  al., 1973; Kitao
266     Jefferson A. Vaughan et al.

et al., 1973). Their original purpose was to determine if black bears, Ursus
americanus (proven earlier to be refractory to SPD), could act as the natural
reservoirs of SPD. Metacercarial-infected trout were fed to six captive bears,
four of which developed fever, anorexia and ‘lassitude’. Upon autopsy, the
sick bears had swollen mesenteric lymph nodes suggestive of salmon poi-
soning. Three of the bears had detectable rickettsial bodies in lymph node
impression smears. Upon injection of individual lymph suspensions from
five autopsied bears into groups of four to six dogs each, 72% of the dogs
developed low-grade fever and diarrhoea for 4–12 days but did not die.
Serial passage of blood during the febrile state into fresh dogs produced
similar, mild symptoms. When convalescent dogs were then fed metacer-
caria-infected trout 3 months later, 87% died of SPD. Because the clinical
symptoms differed and there was lack of conferred immunity between the
two diseases, Farrell et  al. named the disease ‘Elokomin fluke fever’ (EFF)
because the source of the infective trout was the Elokomin River, a tribu-
tary of the Columbia River near its mouth in Washington state. Later stud-
ies confirmed that EFF agent was immunologically distinguishable from
both N. helminthoeca and N. sennetsu (see below) by complement fixation
(Sakawa et  al., 1973), immunofluorescent antibody tests and live animal
challenges (Kitao et  al., 1973). Farrell et  al. (1973) considered EFF and
N. helminthoeca to be a disease complex and indeed the EFF agent has been
provisionally designated as N. elokominica in the Merck Veterinary Manual.
No further work has been published on the EFF agent. Recently, how-
ever, Gai and Marks (2008) reported salmon dog poisoning in two cap-
tive sun bears (U. malayanus) that developed disease upon eating fresh
trout wild caught in Northern California. Both bears developed symp-
toms (vomiting, diarrhoea, anorexia and lethargy) consistent with those
observed in dogs sick with SPD. Foecal samples from sick bears contained
eggs of N. salmincola, the fluke responsible for transmission of SPD. The
authors concluded that the disease was SPD. It can be the case consid-
ering that sun bears as a species presumably have not had exposure to
N. helminthoeca throughout the course of their evolution and may not
have well-pronounced immunity to this disease agent. At the same time,
as mentioned above, it has been experimentally proven that black bears
native to the region do not develop such severe disease upon exposure to
N. helminthoeca. The symptoms described by Gai and Marks (2008) are also
strongly reminiscent of the symptoms described by Farrell et al. (1973) for
the EFF. Thus, it cannot be excluded that the disease described by Gai and
Marks (2008) could have actually been EFF. Since no DNA sequences were
obtained in either case, it is difficult at present to judge on the identity of
these diseases and their respective agents. Regardless, feeding raw salmo-
nid fish from SPD-endemic areas to various species of bears (e.g. sun bears
and polar bears) remains an important veterinary concern for zoos that
maintain captive bears (Bourne et al., 2010).
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     267

3.3.3. Neorickettsia sennetsu and Sennetsu fever

About the same time that early studies on SPD were conducted in the
United States, Japanese scientists were investigating the cause of an acute,
incapacitating rickettsial mononucleosis of humans that had a variety of
local names – Sennetsu, Hyuga or Kagami fevers – endemic to Miyazaki
Prefecture in western Kyushu, Japan (Fukuda et  al., 1954; Misao and
Kobayashi, 1954, 1955; Misao and Katsuta, 1956). Symptoms include
high fever, enlarged postauricular and posterior cervical lymph nodes,
malaise, anorexia and peripheral blood mononucleosis. Hepatospleno-
megaly occurs in some patients. Disease lasts up to 2 weeks; fatalities
are unknown (Misao, Katsuta, 1956; Tachibana, 1986). Epidemiological
studies suggested that the disease is acquired by eating raw grey mullet
fish (Mugil cephalus) infected with metacercariae (Fukuda, 1958). When
96 human volunteers ate metacercaria-infected raw mullet captured from
the Oyodo River, 5 of the volunteers developed clinical symptoms of the
disease (Fukuda et al., 1962). The agent was named Neorickettsia (formerly
Ehrlichia) sennetsu. Neorickettsia sennetsu was isolated from patients and
later from fish, but it was never isolated from metacercariae, nor was the
fluke host ever identified. Later, the agent of this disease was reported
from patients in Malaysia (Holland et al., 1985b; Ristic, 1990; Weiss et al,
1990). Monkeys, rodents and dogs can be successfully infected experimen-
tally and develop multiple symptoms and enlarged lymph nodes (Fukuda
et al., 1954; Ohtaki and Shishido, 1965; Holland et al., 1985b). Interestingly,
the disease has not been reported from Japan for a long time. However,
N. sennetsu was successfully propagated in primary canine blood mono-
cyte cultures that allowed to develop an immunological test that revealed
numerous N. sennetsu infections among patients with fevers of unknown
origin in Malaysia (Holland et al., 1985b).
A recent study (Newton et  al., 2009) revealed that a high seropreva-
lence of N. sennetsu (17% of 1132 patients) occurs in Vientiane municipality
and Savannakhet Province in Laos. Newton et al. (2009) concluded that
sennetsu neorickettsiosis is a common infection in Laos. The same study
showed a 4% seroprevalence in patients in Thailand. It should be noted
that only 1 of 91 buffy coat samples from patients with non-malarious
undifferentiated fever was PCR positive for N. sennetsu. Sequences of PCR
products of three different genes obtained from the human patient sample
were 100% identical to previously published sequences of N. sennetsu
strain Miyayama. Newton et al. (2009) considered it possible that at least
some of the seropositive samples found in their survey resulted from
exposure to organisms closely related to N. sennetsu, but not N. sennetsu.
Laos is a country where raw fish is commonly consumed and fish-borne
intestinal and hepatic digenean infections are prevalent (Chai et al., 2005b,
2007; 2009a, b; Hortle, 2007; Sayasone et al., 2009a, b; Andrews et al., 2008;
268     Jefferson A. Vaughan et al.

TABLE 3.2  Species diversity and worm burden of digenean-infected people living
within two known Neorickettsia sennetsu endemic regions of Laos, 2002–2004

Prevalence of infection (%), mean intensity of infection

Species composition Vientiane (n = 18) Savannakhet (n = 29) Total (n = 47)

Opisthorchis viverrini 100%, 26 76%, 35 70%, 30

Haplorchis taichui 89%, 10 69%, 11 63%, 11
H. pumilio 6%, 1 10%, 18 7%, 9
H. yokogawai 11%, 31 7%, 1 7%, 7
Centrocestus caninus 17%, 1 0%,0 5%, 1
Echinostomatidae spp. 0%, 0 10%, 23 5%, 23
Prosthodendrium 28%, 2 41%, 10 30%, 6
Phaneropsolus bonnei 0%, 0 10%, 8 5%, 8
Dual infections (two 44% 34% 38%
digenean species)
Polyparasitism (three or 44% 31% 36%
more digenean spp.)
(data from Chai et al., 2005b, 2007)

Rim et al., 2008; Table 3.2). Therefore, Newton et al. (2009) screened local
fish for Neorickettsia using standard and real-time PCR (RT-PCR) targeting
the 16S rRNA gene. After screening 238 samples and impressive 88 fish
species including 10 fish species most commonly consumed in and around
the Laos capital Vientiane, Newton et  al. (2009) discovered Neorickettsia
infections in three fish species, namely the dwarf snakehead fish (Channa
gachua), the croaking gourami (Trichopsis vittata) and the climbing perch
(Anabas testudineus). While the sequences from the first two fishes were
significantly different from the sequence of N. sennetsu (92.2% and 95.8%
homology), the sequence from A. testudineus showed 99.1% homology with
the previously published sequence of N. sennetsu strain Miyayama. The
results were confirmed with RT-PCR using two additional genes frequently
used in Neorickettsia systematics, namely gltA and Omp85. Newton et  al.
(2009) presented a phylogenetic analysis showing that the samples from
the human patient and A. testudineus clustered together with N. sennetsu.
Sequences from the other two fish species (C. gachua and T. vittata) were
positioned basal to all Neorickettsia. These recent findings of up to four new
forms of Anaplasmataceae in fish from the same region by Newton et al.
(2009) and Seng et al. (2009) clearly indicate that there is yet much to be
learnt about these bacteria, their diversity and diseases caused by them.
Coincidentally with the study of Newton et  al. (2009), scientists in
the Korean–Laos Cooperation Project on Parasite Control in Lao PDR
­conducted extensive parasitological surveys along the Mekong River,
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     269

including four villages in Vientiane and four villages in Savannakhet

Province (Chai et  al., 2005a, b, 2007). Their survey revealed that 62% of
1580 examined people had active digenean infections. Combining the anti-
Neorickettsia serology and the digenean prevalence data suggests that 27%
of the digenean infections that occurred in Vientiane and Savannakhet
Provinces during 2001–2003 could have resulted in neorickettsioses – i.e.
17% overall anti-sennetsu seropositivity (Newton et al., 2009) divided by
62% overall digenean parasitism (Chai et al., 2005b,s 2007). It means that
over a quarter of all food-borne digenean infections in these two ­Laotian
provinces could have resulted in neorickettsioses.
The Korean–Laotian collaborative study found at least seven digenean
species present and 75% of infected people were parasitized by more than
one digenean species (Table 3.2). Most infected people harboured a few
dozen flukes, while some others harboured hundreds, even thousands.
Although the relative contribution of species varied by location, three spe-
cies dominated in all locations – a liver fluke, Opisthorchis viverrini (Opis-
thorchiidae) and two intestinal flukes, Haplorchis taichui (Heterophyidae)
and Prosthodendrium molenkampi (Lecithodendriidae). The first two are
acquired from eating raw fish (Chai et  al., 2009b). The third species,
Pr. molenkampi, uses dragonfly nymphs as second intermediate host
(Manning and Lertprasert, 1973). Taking into account that insects are
known to host other species/genotypes of Neorickettsia, it cannot be
excluded that arthropods may represent another potential source of
human neorickettsial infections. Considering the extremely widespread
consumption of raw or undercooked fish products in the region, as well as
common use of various invertebrates (crustaceans, insects and molluscs)
as food (Chai et  al., 2005a, b; Hortle, 2007), human neorickettsioses are
probably more common in this part of the world than currently known.
Nearly nothing is known about distribution of N. sennetsu among
mammals other than humans, with the exception of a single report from
rodents in Japan (Fukuda et  al., 1962). Taking into account the known
pathogenicity of N. sennetsu in some non-human mammals resulting
from experimental infections (see above), it cannot be excluded that this
agent may cause disease in wild animals as well. Unfortunately, our
knowledge of the ecology of N. sennetsu and other related genotypes is
rather marginal. The thorough study done by Newton et al. (2009) that
resulted in multiple records of Neorickettsia in fish did not incriminate
any digenean species. Considering the extremely diverse traditional
diets in the region, more Neorickettsia transmission pathways are possible
than merely through fish. The case of N. risticii that can infect a variety
of digeneans having diverse life cycles (see Section 3.3.4 of this review),
from entirely aquatic to entirely terrestrial, provides a clue that the cir-
culation of Neorickettsia in nature may be more flexible than we currently
270     Jefferson A. Vaughan et al.

3.3.4. Neorickettsia risticii and PHF

In the late 1970s, a mysterious, summertime illness of horses appeared
in the rural counties of Maryland and Virginia surrounding Washing-
ton, DC. Clinical symptoms varied, but usually included fever (often
biphasic), depression, anorexia and colitis (inflammation of large colon),
accompanied by acute diarrhoea (Holland et  al., 1985c; Rikihisa, 1991).
In severe cases, horses exhibited laminitis. Pregnant mares often aborted
(Coffman et al., 2008, Long et al., 1995). If left untreated, overall mortality
approached 30% (Cordes et al. 1986). The clinical term for this condition
is equine monocytic ehrlichiosis but because the initial cases occurred in
horses pastured close to the Potomac River, the disease became known
as ‘Potomac horse fever’ (PHF). Stools from diarrhoeic horses contained
the infectious agent and, when fed to susceptible horses, could produce
PHF (Biswas et al., 1994, Palmer and Benson, 1994). However, the highly
seasonal occurrence of the disease, coupled with the fact that susceptible
horses stabled with sick horses rarely acquired PHF, suggested that PHF
was not a communicable disease but instead was a vector-borne disease.
The causative organism was initially placed in the genus Ehrlichia
(Holland et al., 1985a, c; Rikihisa and Perry, 1985). This led to some early
confusion regarding the transmission of PHF because Ehrlichia are known
to be tick borne. However, vector competence studies at the time failed to
incriminate local tick species in the transmission of the PHF (Hahn et al.,
1990, Levine et al., 1990).
The source of PHF remained enigmatic for years, until advances in molec-
ular biology transformed bacterial systematics in the early 1990s. When
Yasuko Rikihisa and her team at Ohio State University applied molecular
methodology to the study of ehrlichial diseases, they not only accelerated
the development of accurate diagnostic tools for PHF (Messick and Riki-
hisa, 1992a, b; Barlough et al., 1997, Mott et al., 1997a, b; Pusterla et al., 2006)
but importantly, their efforts as well as others, allowed for the phylogenetic
reconstruction of the Rickettsiales (Pretzman et al., 1995; Dumler et al., 2001;
Inokuma et al., 2001). As a result of this landmark accomplishment, it became
evident that the PHF agent was phylogenetically closer to the fluke-borne
agents of SPD, sennetsu fever and the SF agent than it was to tick-borne
ehrlichiae. This proved to be a textbook example of the utility of systemat-
ics and phylogenetics in resolving pressing practical questions related to a
new emerging disease and it provided the clue that enabled the University
of California (UC) Davis veterinarian team of John Madigan and colleagues
to begin to put the pieces of the PHF puzzle together (Dumler, 2000).
Using PCR technology, the UC Davis team isolated N. risticii DNA
from small pleurocercid snails ( Juga spp.) collected in the streams of an
endemic area (Barlough et al., 1998; Reubel et al., 1998). When cercariae
and ­sporocysts from fluke-infected snails were inoculated into horses, the
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     271

horses became ill with PHF (or Shasta River crud, as it is known locally;
Madigan et  al., 1997). Neorickettsia risticii were recovered from buffy
coats of the sick horses (Pusterla et al., 2000a, c), satisfying Koch’s postu-
lates. Further studies elucidated the ecology of PHF in northern Califor-
nia (Pusterla et al., 2000a, c, 2003; Chae et al., 2000, 2002) and in central
Pennsylvania (Mott et  al., 2002; Gibson et  al., 2005; Gibson and Riki-
hisa, 2008). Transmission cycles in these areas involve several fluke spe-
cies that use river snails (e.g. Juga) as the first intermediate host, aquatic
insects (e.g. caddisflies and mayflies) as the second intermediate host and
insectivorous birds and/or bats as the definitive hosts (Fig. 3.5). Within
PHF-endemic areas, rates of N. risticii infection in intermediate hosts of
digeneans were high. In northern California, up to 26% of the snails har-
bouring larval digeneans tested PCR positive for N. risticii DNA (Pusterla
et al., 2000a, c). Likewise in central Pennsylvania, 5 of 42 pools (12%) of
cercariae and sporocyts collected from snails tested PCR positive for
N. risticii DNA, as did 2 of 10 pools (20%) of adult mayflies and 3 of 8 pools
(38%) of adult caddisflies (Mott et al., 2002).
To determine if metacercaria-infected insects harboured viable N. risticii,
two horses were fed pools of field-collected caddisflies that had tested
positive for N. risticii. Six to 11 days later, both horses became neorick-
ettsemic and clinically ill with PHF (Mott et  al., 2002). Therefore, trans-
mission in these areas supposedly occurs when horses somehow swallow
insects containing metacercariae. This could occur in a variety of ways –
either through consuming insects while grazing, eating insect-contami-
nated hay, or by drinking insects that have been attracted at night to lights
over watering troughs and fell in the water (Farren, 2007). It is also pos-
sible that horses may acquire PHF by drinking water containing cercariae
shed by snails. To the best of our knowledge, this potential transmission
route has not yet been tested experimentally.
At least two different genera of adult flukes (Acanthatrium sp., Lecithoden-
drium sp.) parasitizing bats and swallows were found to harbour N. risticii
DNA (Pusterla et al., 2003; Gibson et al., 2005; Gibson and Rikihisa, 2008).
Importantly, unparasitized tissues (liver and spleen) from the definitive hosts
also contained N. risticii DNA (Pusterla et al., 2003), suggesting that insec-
tivorous birds and bats may act as natural vertebrate reservoirs of N. risticii.
However, several reports indicate that enzootic transmission cycles of
N. risticii are not necessarily restricted to lotic (i.e. riverine) ecosystems or
to a single type of digenean life cycle (Table 3.3). For example, Barlough
et al. (1998) reported detecting 16S rRNA sequence of N. risticii from a pool
of Stagnicola (Lymnaeidae) snails in Oregon. Stagnicola are common inhab-
itants of ponds and lakes throughout North America and are hosts to repre-
sentatives of many digenean families (Schell, 1985). On the shores of Lake
Merin, Uruguay, Dutra et al. (2001) found a significant clustering of cases
of PHF (=churrido equino) in horses that were regularly pastured in the
272     Jefferson A. Vaughan et al.

low marshy fields bordering the lake (36 per 1000 horse years) compared to
the horses pastured in rice plain fields (3 per 1000 horse years). In our pre-
liminary surveys, N. risticii DNA was isolated from two different species of
cercariae shed from Helisoma trivolis snails (Planorbidae) collected at Lake

FIGURE 3.5  Circulation of Neorickettsia risticii (white dots) involving lecithodendriid

digeneans (e.g. Acanthatrium spp.) and horses as a dead-end host. Images of snail and
fish are by T. Dieter and T. Saxby, Integration and Application Network, University of
Maryland Center for Environmental Science ( Images of
animals are by T. Dieter (snail, mayfly larva), T. Saxby (bat, horse) and K. Kraeer and L.V.
Essen-Fishman (mayfly adult), Integration and Application Network, University of
Maryland Center for Environmental Science ( (For color
version of this figure, the reader is referred to the web version of this book.)
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     273

Itasca, MN, USA (Table 3.3). Taken together, these observations ­indicate
that natural transmission of N. risticii may also involve lentic (=lake and
pond) ecosystems.
Moreover, N. risticii DNA has been recovered from an adult dicrocoe-
liid fluke parasitisizing a small passerine bird in North Dakota, USA (V.V.
Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data). This is sig-
nificant because all dicrocoeliid flukes utilize land snails or slugs as their
first intermediate hosts and terrestrial invertebrates (usually arthropods)
as second intermediate hosts (Yamaguti, 1975; Schell, 1985). In addition,
we (V.V. Tkach, J.A. Schroeder and J.A. Vaughan, unpublished data) have
recently detected by PCR and sequenced N. risticii in digeneans with fully
aquatic life cycles, namely Alloglossidium corti (parasite of catfishes; Table 3.3)
and Heronimus mollis (parasite of freshwater turtles; Table 3.3). The for-
mer uses arthropods as second intermediate hosts, while the latter does
not have a second intermediate host and metacercariae remain within the
snail until eaten by a turtle. Thus, N. risticii is present in various digenean
groups having all of the main types of life cycles typical of freshwater/
terrestrial ecosystems (Fig. 3.6). Thus far, N. risticii has not been reported
from marine or estuarine environment. These findings demonstrate the
great plasticity of N. risticii circulation pathways in nature (Fig. 3.6). All
this indicates that enzootic transmission cycles of PHF occur even in many
ecosystems, even fully terrestrial ecosystems, which explains how horses

FIGURE 3.6  Generalized circulation pathways of Neorickettsia risticii based on life

cycles of its currently known digenean hosts. (For color version of this figure, the reader
is referred to the web version of this book.)
274     Jefferson A. Vaughan et al.

contract PHF in pastures far removed from rivers, streams, lakes or ponds.
Thus, the risk of horses contracting PHF may be more widespread than
previously recognized.
We are not aware of any studies demonstrating the presence of adult
flukes in horses that have contracted PHF. Indeed, the digenean fauna of
horses is generally very poor, and thus far, none of the digenean species
from which N. risticii DNA has been recovered belonged to groups that
can develop to the adult stages in horses. Thus, it appears that digenean
metacercariae do not need to complete development to the adult stage in
order to pass the infection to horses. Unlike the situation with SPD and
dogs, horses can truly be considered ‘dead-end hosts’ for PHF transmis-
sion. It remains unknown whether all species of N. risticii-infected meta-
cercariae ingested by a horse can lead to PHF or whether only certain
species or groups of digeneans can successfully transmit their neorickett-
sial endosymbionts before being destroyed in the horse’s digestive system
or expelled with the droppings.
A commercial vaccine for PHF based on the type strain, N. risticii Illi-
nois, became available in the late 1980s. However, soon afterwards, cases
of vaccine failures began to surface (Vemulapalli et al., 1995, Dutta et al.,
1998), suggesting that there were other, naturally occurring strains of
N. risticii that could infect horses but were different antigenically from the
strain upon which the vaccine was based. Various studies have supported
the idea of strain variation within N. risticii. In an early study examin-
ing this issue, Chaichanasiriwithaya et al. (1994) compared Western blot
and monoclonal antibody reactivity profiles of nine isolates collected in
Ohio and Kentucky from horses experiencing acute, naturally acquired
PHF. Three of the horses represented cases of ‘vaccine failure’ as they had
been vaccinated against PHF 6 months earlier and had high levels of anti-
N. risticii antibodies. From this relatively small sample size from a rela-
tively narrow geographic region, Chaichanasiriwithaya et al. (1994) found
three immunologically distinct N. risticii ‘sero-groups’. More recently,
Gibson et al. (2011) reported a strong geographic clustering among various
N. risticii isolates collected in the United States with respect to the pre-
dicted amino acid sequences of several proteins, including two external
loops of the major immunodominant surface-expressed protein, p51. The
cause of such variation is not known but is unlikely to be the result of
selective pressure placed on the bacteria by humoral responses of infected
horses. Neorickettsia are intracellular and horses represent a dead-end for
further Neorickettsia transmission. Rather, Gibson et al. (2011) speculated
that strain variation in N. risticii may be related to the specific type of dige-
nean harbouring the endosymbiont. The data provided by Gibson et al.
(2011) support earlier suggestions by Barlough et  al. (1998) and Reubel
et al. (1998) that N. risticii actually constitutes a collection of strains that
may differ in the digenean hosts, snail ecology and virulence to horses.
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     275

As more information regarding strain variation accumulates over

broad geographic regions and the principal digenean hosts involved in
local transmission are identified, it may be possible to detect patterns
in digenean/endosymbiont strain associations and thereby define site-
specific ecologies of transmission. If such associations exist and can be
mapped out, then preventive strategies can be tailored to specific regions
to limit horse exposure to N. risticii-infected metacercariae and thus reduce
the administration of ineffectual vaccines or the over reliance on antibiot-
ics to prevent and treat PHF (Kanter et al., 2000).

3.3.5. SF agent

During the search for the agent of sennetsu fever, another neorickettsial
agent was discovered in S. falcatus metacercariae infecting grey mullet and
has been consistently found during at least 17 years of regular studies
(Fukuda et al., 1973; Fukuda and Yamamoto, 1981). The agent has become
known as ‘SF agent’ (short for ‘Stellantchasmus falcatus agent’) and differs
from N. sennetsu in western blot profiles probed with anti-SF sera, clinical
and pathologic responses of mice and 16S rRNA sequence comparisons
(Wen et al., 1996). The SF agent is not known to cause disease in humans
or in experimentally infected monkeys. It produces splenomegaly and
lymphadenopathy when injected into mice but produces only mild clini-
cal symptoms in dogs (Shishido et  al., 1965; Hirai, 1966; Fukuda and
Yamamoto, 1981; Tachibana, 1986; Rikihisa, 1991; Wen et al., 1996). This
genotype of Neorickettsia can be maintained by mouse passages in labora-
tory (Fukuda and Yamamoto, 1981). Its digenean host, S. falcatus has a
snail/fish/mammal type of life cycle associated with lotic/estuarine habi-
tats. When ingested by humans, S. falcatus metacercariae are able to mature
to the adult stage in the intestine (Katsuta, 1931; Seo et al., 1984). Infection
with this small heterophyid fluke is of minor medical concern, causing
only mild intestinal discomfort and occasional diarrhoea (Seo et al., 1984).
Despite the wide geographic range of this fluke species (Japan, Korea,
Southeast Asia, Hawaii, Australia, Egypt, Palestine and Israel according to
Katsuta, 1931; Pearson, 1964; Chai and Sohn, 1988), SF agent has only been
recorded from Japan (Fukuda et al., 1973; Wen et al., 1996). It is not known
if it may inhabit other digenean species or other vertebrate animals.

3.3.6. Rainbow trout agent

During the studies to elucidate the ecology of PHF in California, 35 rain-
bow trout were collected from the Shasha River in a PHF-endemic area.
Neorickettsial DNA was recovered from three species of adult digenean
parasites collected from the gall bladder and intestine of the trout (Crep-
idostomum, Creptotrema, Deropegus spp.) and from the eggs of a blood fluke
276     Jefferson A. Vaughan et al.

(Sanguinicola sp.) recovered from gill capillaries (Pusterla et  al., 2000b).
Neorickettsial DNA was also recovered from unparasitized fish tissues,
which may have represented either neorickettsial infection of host blood/
tissue or infection by undetected blood fluke eggs. Sequences of the ampli-
cons of 16S rRNA gene obtained from fish tissue and flukes were identical
to each other and very close to the sequences of members of Neorickettsia.
At the same time, they were distinct enough from N. risticii, N. sennetsu,
SF agent and N. helminthoeca (95–96% sequence homology) to suggest
that the ‘rainbow trout agent’ is a previously unrecognized genotype of
Neorickettsia. Nothing is known about its pathogenicity in fish or in verte-
brates that eat fish.

3.3.7. Neorickettsia sp. from needlefish in Cambodia

Seng et al. (2009) studied frozen fish and fish-based ingredients imported
from Thailand, Vietnam and Cambodia to Asian markets in Marseille,
France. They examined fish digestive tracts for parasitic worms and subse-
quently extracted DNA from digestive tracts. For detection of Anaplasma-
taceae, they used PCR with primers specific for the 16S rRNA and citrate
synthase genes of this group of bacteria. Three different forms of Ana-
plasmataceae were determined in the fish digestive tracts. Based on the
level of the sequence homology, the authors suggested that two of them
represented new genera within the Anaplasmataceae, while the third rep-
resented a new species of Neorickettsia. To define specific and generic lev-
els of sequence divergence in the Anaplasmataceae, the authors chose a
threshold of 97% identity among homologous 16S rRNA gene sequences
generated from each isolate. In a phylogenetic tree of the Anaplasmata-
ceae, the three genotypes all clustered together with Neorickettsia. The
two new genera were basal to all Neorickettsia, while the third belonged
to the clade containing the rainbow trout agent (Fig. 3.2). The new Neor-
ickettsia sp. was found in a freshwater needlefish Xenentodon cancila from
Cambodia. No digeneans were found in the needlefish, thus, the potential
­circulatory pathway of these neorickettsiae remains unknown.

3.3.8. Catfish agents

Recently, we isolated two genotypes of Neorickettsia from different dige-
neans parasitic in catfishes in the United States (V.V. Tkach, J.A. Schro-
eder and J.A. Vaughan, unpublished data). These genotypes showed high
sequence homology (95–98%) with members of Neorickettsia and belonged
to two different clades within the genus (Fig. 3.3). One of them was
obtained from a gorgoderid digenean, Phyllodistomum lacustri, found in
the bladder of a stonecat catfish (Noturus flavus) and tentatively called cat-
fish agent 1. The other was obtained from an allocreadiid digenean, Megal-
ogonia ­ictaluri, found in the intestine of channel catfish (Ictalurus punctatus)
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     277

and tentatively called catfish agent 2. The former genotype seems closest
to N. helminthoeca, while the latter clustered with the published sequence
of the rainbow trout agent (Fig. 3.3). These findings, combined with dis-
coveries of the ‘EFF agent’ and rainbow trout agent, suggest that a rela-
tively diverse Neorickettsia species/genotype complex exists in digenean
parasites of North American freshwater fish.
These forms deserve more detailed studies, especially in view of the fact
that the catfish agent 2 was recovered from a digenean species parasitic in
the channel catfish – an important fish species that is raised commercially
and packaged for sale and consumption throughout the United States and
elsewhere. Worldwide, the channel catfish production has increased steadily
and has reached well over 450,000 tons per year according to Food and
Agriculture Organization fishery statistics (
culturedspecies/Ictalurus_punctatus/en). Therefore, while the public health
importance of this and other poorly characterized Neorickettsia genotypes
is unclear, these discoveries nevertheless indicate that, even in the United
States, neorickettsiae occur dangerously close to the human food chain.


There are reports of confirmed or probable neorickettsial infections from

all continents, with N. risticii being by far the most widely distributed
and most frequently reported species of Neorickettsia (Dumler et al., 2005).
However, the majority of these reports including all information available
from Europe, Africa, Australia, as well as some Asian (e.g. India) and South
American (e.g. Venezuela) countries is based exclusively on serological test-
ing of horses without further evidence from either PCR/sequencing or cul-
turing the bacteria. In most cases, the vaccination or relocation histories of
serologically positive horses were not known or reported. Clearly, serolog-
ical tests have limitations and depend on previous exposure whether from
natural infections or vaccinations. Madigan et al. (1995) provided convinc-
ing evidence of high rate of false-positive results when the most common
serological diagnostic tool, the indirect fluorescent antibody (IFA) test, was
used to diagnose PHF in California. Later, Mott et al. (1997a) compared rel-
ative sensitivity and usability of IFA versus nested PCR while concurrently
culturing bacteria in the majority of samples. At the time, horses with sero-
logic evidence of prior exposure to PHF were found throughout the United
States, Canada and Europe, and seroepidemiological studies reported high
seroprevalences of horses that lacked clinical symptoms of PHF. However,
culture of N. risticii was rarely done and most of the diagnoses were based
on IFA testing. Mott et al. (1997a) emphasized that IFA testing at a single
time point is useless as a surveillance tool for detecting PHF in vaccinated
horses and expressed the same concern as Madigan et al. (1995) regarding
278     Jefferson A. Vaughan et al.

the reliability of reports based on serological evidence alone. Mott et  al.
(1997a) concluded that the PCR test was as accurate and sensitive as cul-
turing and has an advantage over the IFA test because it is independent
of the past vaccination history of a horse. Therefore, in this section and on
the map in Fig. 3.7, we consider only data resulting from application of
PCR/sequencing techniques or culturing of the bacteria. Exceptionally, we
consider a few cases when sufficient vaccination/relocation histories were
reported for individual serologically positive horses.
Even after applying the stricter criteria outlined above, N. risticii
remains the most widely distributed species/genotype of Neorickettsia
(Fig. 3.7; Tables 3.1 and 3.3). It is broadly distributed throughout North
America and was recently reported from Brazil and Uruguay (Fig. 3.7).
Korean researchers (Chae et al., 2003; Park et al., 2003) also reported N. ris-
ticii from larval stages of several digenean species in the Republic of Korea.
However, the relatively high level of 16S sequence divergence between
Korean isolates and those from the United States suggests that the species
identity of the Korean genotype should be considered with some caution
(see discussion in Section 3.2.2 of this review). In any case, one or another
Neorickettsia species is certainly distributed in the Republic of Korea.
Another species of Neorickettsia that seems to be rather broadly distrib-
uted is N. helminthoeca that was long known to cause dog disease in the
Pacific northwest of the United States but then was found in other parts of
the western coast of North America, from British Columbia to California
(Booth et al., 1984; Sykes et al., 2010) as well as in Brazil (Headley et al.,
2004, 2009). The third named Neorickettsia species, N. sennetsu, is the most
widely distributed member of the genus in Asia and was found so far in
Japan, Malaysia, Laos and Thailand. All remaining five Neorickettsia geno-
types have very limited distribution and have been found in a single geo-
graphical area each (Fig. 3.7), either in North America, Japan or Southeast
Asia. Invariably, these genotypes have been discovered as a by-product of
studies targeting pathogenic species.
Thus, the known confirmed distribution of Neorickettsia is very uneven
from the geographical viewpoint. If we use the conservative approach out-
lined above, well-documented information on Neorickettsia is lacking from
Africa, Australia, Europe, most of South America, most of Asia and nearly
all island countries. In our opinion, this patchy distribution reflects a lack
of studies and insufficient knowledge rather than the true absence of Neor-
ickettsia from most regions of the planet. As far as we are aware, there were
no studies focusing on finding Neorickettsia anywhere in Africa or Austra-
lia. At the same time, already proven Neorickettsia symbiosis in representa-
tives of all major phylogenetic lineages of the Digenea (see Section 3.5 of
this review) suggests that these bacteria may likely be widely distributed
geographically. It is probably not accidental that the species with widest
distribution are those of significant veterinary or medical importance. It
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution    
FIGURE 3.7  Geographic distribution of known species and genotypes of Neorickettsia. Records based solely on serological diagnostics are not
included. (For color version of this figure, the reader is referred to the web version of this book.)

TABLE 3.3  Known digenean hosts of Neorickettsia species/genotypes their natural definitive hosts and geographic origin of Neorickettsia-

positive samples

Neorickettsia Digenean genus Digenean

species Digenean family and species definitive host Life cycle Country Reference

Jefferson A. Vaughan et al.

Neorickettsia Troglotrematidae Nanophyetus Marine and Aquatic/ United States Philip et al. (1953)
helminthoeca salmincola freshwater terrestrial
EEF agent Troglotrematidae N. salmincola Marine and Aquatic/ United States Farrell et al. (1973)
freshwater terrestrial
Neorickettsia Dicrocoeliidae Conspicuum sp. Birds Terrestrial United States V.V. Tkach, J.A.
risticii Schroeder and J.A.
Vaughan, unpublished
Echinostomatidae Echinoparyphium Birds Aquatic/ United States V.V. Tkach, J.A. Schroeder
rubrum terrestrial and J.A. Vaughan,
Echinostomatidae Echinostoma Mammals Aquatic/ South Korea Park et al. (2003)
cinetorchis (humans) terrestrial
Echinostomatidae Echinostoma Birds and Aquatic/ South Korea Park et al. (2003)
hortense mammals terrestrial
Fasciolidae Fasciola sp. Mammals Aquatic/ South Korea Park et al. (2003)
Heronimidae Heronimus mollis Freshwater Aquatic United States V.V. Tkach, J.A. Schro-
turtles eder and J.A. Vaughan,
Lecithodendriidae Lecithodendrium sp. Mammals Aquatic/ United States Pusterla et al. (2003)
and birds terrestrial
Lecithodendriidae Acanthatrium sp. Mammals Aquatic/ United States Pusterla et al. (2003)

Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution    

(bats) terrestrial
Lecithodendriidae Acanthatrium orego- Mammals Aquatic/ United States Gibson et al. (2005)
nense (bats) terrestrial
Macroderoididae Alloglossidium corti Freshwater Aquatic United States V.V. Tkach, J.A.
fish Schroeder and J.A.
Vaughan, unpublished
Microphallidae Microphallidae sp. Bird or Aquatic/ South Korea Park et al. (2003)
mammal terrestrial
Plagiorchiidae Plagiorchis elegans Birds and Aquatic/ United States S.E. Greiman and V.V.
mammals terrestrial Tkach, unpublished
Schistosomatidae Schistosomatidae Birds and Aquatic/ South Korea Park et al. (2003)
sp. mammals terrestrial
Neorickettsia Not known Not known Not known Not known Japan, Fukuda et al. (1954);
sennetsu Malaisia, Misao and Kobayashi
Laos, (1954)
Neorickettsia Gorgoderidae Phyllodistomum Freshwater Aquatic United States V.V. Tkach, J.A.
sp. (catfish lacustri fish Schroeder and J.A.
agent 1) Vaughan, unpublished
Neorickettsia Allocreadiidae Megalogonia ictaluri Freshwater Aquatic United States V.V. Tkach, J.A.
sp. (catfish fish Schroeder and J.A.
agent 2) Vaughan, unpublished

TABLE 3.3  (Continued)

Neorickettsia Digenean genus Digenean
species Digenean family and species definitive host Life cycle Country Reference

Jefferson A. Vaughan et al.

Neorickettsia Not known Not known Freshwater Not known Cambodia Seng et al. (2009)
sp. fish
Neorickettsia Derogenidae Deropegus sp. Freshwater Aquatic United States Pusterla et al. (2000)
sp. (rain- fish
bow trout Allocreadiidae Crepidostomum sp. Freshwater Aquatic United States Pusterla et al. (2000)
agent) fish
Allocreadiidae Creptotrema sp. Freshwater Aquatic United States Pusterla et al. (2000)
Sanguinicolidae Sanguinicola sp. Freshwater Aquatic United States Pusterla et al. 2000
Neorickettsia Heterophyidae Stellantchasmus Mammals Aquatic/ Japan Fukuda and
sp. (SF falcatus (humans) terrestrial Yamamoto (1981)
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     283

reflects the fact that much more resources have been put into studies of
these species. An additional important factor might be the high mobil-
ity of humans and high frequency of relocation of domestic animals that
could facilitate the spread of some of the Neorickettsia genotypes. Available
evidence suggests that PHF was almost certainly historically absent from
North America. Considering the vital importance of horses to the economy
and culture of early settlement of North America, it seems strange that PHF
had never before been diagnosed as a recognizable disease prior to 1970.
It would be difficult to expect that a disease with visible clinical symp-
toms would have gone completely unnoticed for centuries. As it turns out,
N. risticii has been identified as the causative agent for ‘churrido equino’ –
a diarrhoeic disease of horses known for over 100 years in the Lake Merin
region of Uruguay and Brazil (Dutra et  al., 2001; Coimbra et  al., 2005).
We hypothesize that PHF might have been introduced to North America
from South America relatively recently. Comparative phylogenetic studies
of a greater number of samples from as broad geographic area as possible,
optimally using sequences of several genes, may provide some insight into
this interesting question and either confirm or refute this hypothesis.
Obviously, there are natural causes for differences in the distribution
of various Neorickettsia species/genotypes. For instance, the most widely
spread species, N. risticii, is the only one found so far in flying migratory
vertebrate animals (birds and bats), which may have an impact on the
distribution of their digeneans and digenean endosymbionts. The most
obvious mechanism limiting the geographic distribution of the majority of
Neorickettsia genotypes is related to the specificities of the bacteria to their
fluke hosts on the one hand and of flukes to their intermediate and defini-
tive hosts on the other. Most digeneans are rather tightly ecologically and
evolutionarily associated with their mollusc hosts as well as other host cat-
egories (Yamaguti, 1975; Cribb et al., 2001, 2003). It means that if even one
of the hosts in the digenean complex life cycle has a limited distribution,
it will limit the distribution of the fluke species. Nanophyetus salmincola
is a good example of such dependency due to its high specificity to a mol-
lusc host with a limited geographic distribution (see Section 3.3.1).
As studies of neorickettsiae are undertaken in new regions, we antici-
pate that the known geographic distribution of these endosymbionts will
expand significantly.


Neorickettsiae are widely distributed among digeneans. In fact, one or
another species or genotype of these endosymbionts is found in represen-
tatives of all major lineages of the Digenea (Fig. 3.8). Some neorickettsial
284     Jefferson A. Vaughan et al.

FIGURE 3.8  Neorickettsia species/genotype records mapped on the phylogenetic tree

of the digenan families from Olson et al. (2003; published by permission from Elsevier).
Records of Neorickettsia obtained from published data and unpublished data by V.V.
Tkach, J.A. Schroeder and J.A. Vaughan (Table 3.3). A record in Alloglossidium corti is not
shown on the tree because the Allocreadiidae were not included in the phylogenetic
analysis by Olson et al. (2003).
Neorickettsial Endosymbionts of the Digenea: Diversity, Transmission and Distribution     285

species seem to have a narrow host range, restricted to within a single

family of Digenea (e.g. salmon poisoning, EFF agent and SF agent;
see Fig. 3.8). Other neorickettsial species have been isolated from phy-
logenetically distant digenean families (e.g. rainbow trout agent; see
Fig. 3.8). Neorickettsia risticii displays the broadest digenean host utiliza-
tion, with its DNA having been isolated from an astonishing diversity of
digeneans including a range of families from one of the most basal dige-
nean lineages (Schistosomatidae and Strigeidae) to the most advanced lin-
eages (Lecithodendriidae and Microphallidae). This may indicate that the
neorickettsiae as a group have had a long evolutionary history with Digenea
and suggests that neorickettsiae may be potentially found in many addi-
tional groups of Digenea. At the same time, there is no evidence of clear
coevolutionary relationship between certain digenean lineages and their
bacterial endosymbionts. For example, identical sequences of 16S rRNA
have been obtained from widely divergent digenean taxa. Conversely,
different genotypes producing different pathologies in dogs and bears,
i.e. N. helminthoeca and EFF agent, share the same digenean host species,
N. salmincola.
The exact nature of the endosymbiotic relationship among neorickett-
siae and their digenean hosts at physiological level is currently unclear. It
is likely not obligatory because there is no apparent dependency of digene-
ans on these endosymbionts. Some individuals within the same digenean
species may be infected with neorickettsiae, whereas other individuals are
not. This situation is different, for instance, from the obligatory relation-
ships among Wolbachia and certain species of filariid nematodes (Taylor
et al., 2005; Casiraghi et al., 2005; Ferri et al., 2011; Fischer et al., 2011). The
potential influence of Neorickettsia on their digenean hosts remains practi-
cally unknown and represents one of the most interesting aspects of their



Most of the advances in our knowledge of the biology, host associations

and distribution of Neorickettsia in the last 15–17 years are intimately
linked to the development of molecular approaches and techniques,
particularly PCR and DNA sequencing. As mentioned before, use of DNA
sequences has revolutionized the systematics and phylogenetics of this
group of bacteria. Although 16S rRNA region remains the primary tar-
get for both diagnostics and phylogenetic analyses (Pretzman et al., 1995;
Dumler et al., 2001; Stackebrandt et al., 2002; Headley et al., 2011), several
other genes have been proposed and used for both diagnostics and phylo-
genetics, e.g. the citrate synthase gene (gltA; Inokuma et al., 2001; Rikihisa
286     Jefferson A. Vaughan et al.

et al., 2004), the RNA polymerase b-subunit (Taillardat-Bisch et al., 2003),

the heat shock protein gene (groESL; Dumler et al., 2001; Rikihisa et al.,
2004; Headley et al., 2011), the p51 gene encoding major antigenic 51-kDa
protein (Rikihisa et al., 2004) and the outer membrane protein Omp85 gene
(Newton et al., 2009). The groESL gene is the second most widely utilized DNA
region utilized in differentiation among lineages and species of Neorickettsia.
With further evolution of PCR technology, use of RT-PCR including
TaqMan probes provided an additional convenient method for quick and
reliable detection of Neorickettsia (Pusterla et al., 2006; Newton et al., 2009).
Complete genomes of several Anaplasmataceae were recently pub-
lished, including two annotated genomes of Neorickettsia, namely N. sennetsu
(Hotopp et al., 2006) and N. risticii (Lin et al., 2009). Hotopp et al. (2006)
conducted a comparative analysis of genomes of 19 obligate and faculta-
tive intracellular pathogenic and endosymbiotic bacteria and discovered
that 176 orthologue clusters (mostly with housekeeping functions) are
conserved across these bacterial lineages. Members of the Anaplasmata-
ceae had significantly higher percentages of their genomes dedicated to
nucleotide biosynthesis, cofactor and vitamin biosynthesis, and protein
synthesis than did free-living α-proteobacteria.
Neorickettsiae have the smallest genome size of all members of the Ana-
plasmataceae examined to date. The annotated genome of N. risticii consists
of 879,977 bp and encodes 38 RNA species and 898 proteins (Lin et al., 2009).
Genome-wide comparison between N. risticii and N. sennetsu showed that
very high percentage (758 or 88.2%) of protein-coding genes is conserved
between N. risticii and N. sennetsu. Moreover, comparison of genes among N.
risticii and other Anaplasmataceae showed that most genes (525 orthologs
generally associated with housekeeping functions) are shared among other
members of major Anaplasmataceae lineages. Besides other obvious poten-
tial uses of this information, it suggests that many more genes are available
for species differentiation and phylogenetic inference in this group than cur-
rently used. On the other hand, Lin et al. (2009) showed that some genes of
N. risticii and N. sennetsu have greater homology to those of α-proteobacteria
than to the same genes in other Anaplasmataceae, including the genes cod-
ing for histone-like HU DNA-binding proteins, adenosine triphosphate syn-
thase subunits, DsbB/D protein and some ribosomal protein subunits.
Certain genes potentially involved in the pathogenesis of N. risticii have
been identified, including those encoding putative outer membrane pro-
teins, two-component systems and a type IV secretion system. The genome
of N. risticii encodes for a fully functional aerobic respiratory pathway but
encodes for only a partial glycolytic pathway. Although N. risticii has lim-
ited ability to synthesize amino acids and lacks many metabolic pathways,
it is capable of making major vitamins, cofactors and nucleotides. Like
in other anaplasmids, the Neorickettsia genome does not encode for pep-
tidoglycan or lipopolysaccarhide synthesis, which are potent