Fungal Ecology xxx (2015) 1e10

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Fungal Ecology
journal homepage: www.elsevier.com/locate/funeco

Biogeography of aquatic hyphomycetes: Current knowledge and

future perspectives
rlocher b, Cla
udia Pascoal a, Fernanda Ca
ssio a
Soa Duarte a, *, Felix Ba
a
b

Centre of Molecular and Environmental Biology (CBMA), Department of Biology, University of Minho Campus de Gualtar, 4710-057 Braga, Portugal
Department of Biology, Mount Allison University, Sackville, New Brunswick E4L 1G7, Canada

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 2 March 2015
Received in revised form
26 May 2015
Accepted 5 June 2015
Available online xxx

Since Ingold's (1942) initial description, mycologists have been interested in deciphering global distribution patterns of aquatic hyphomycetes, a group of fungi that play a key role in plant-litter decomposition in freshwaters. However, many questions remain largely unanswered. In this review, we used
distribution data of morphospecies from studies throughout the world in an attempt to better understand the magnitude of global species richness, patterns of biodiversity and the extent of cosmopolitanism versus endemism. Sampling efforts have varied among geographic regions, and correlate
signicantly with species richness. Community similarity decreased with geographic or latitudinal distance. Species richness was highest at mid-latitudes (temperate streams), and high community similarities were found between geographically distant locations in similar climatic zones. Studies relying on
morphotypes have undoubtedly provided relevant information on the geographic distribution of aquatic
hyphomycetes. However, metagenomic approaches combining taxonomic, phylogenetic and functional
diversity in coordinated surveys will be the best option to better decipher diversity patterns of these
fungi and their functional roles at a global scale.
2015 Elsevier Ltd and The British Mycological Society. All rights reserved.

Keywords:
Aquatic hyphomycetes
Biogeography
Phylogeography
Metagenomics
Morphospecies
Genetic diversity
Next-generation sequencing

1. Introduction
Fungi are widely distributed across all biomes and play a major
role in the recycling of organic matter with more than 600 species
reported from freshwaters (Wong et al., 1998; Shearer et al., 2007).
Ingoldian fungi or aquatic hyphomycetes abound in well-aerated
waters and are regarded as the dominant microbial decomposers
rlocher, in this issue). Members of
of leaves decaying in streams (Ba
this ecologically dened group regularly sporulate under water,
and have large conidia (often spanning more than 50 mm) of two
predominant shapes: branched and often tetraradiate or multiradiate (stauroid), and sigmoid or worm-like (scolecoid) (Gulis
et al., 2005; Shearer et al., 2007) (Fig. 1). Much of our knowledge
on aquatic hyphomycete diversity in freshwaters emerges from
species classication based on their characteristic conidial shapes.
Though slightly heavier than water, conidia are readily trapped in
foam or scum, which accumulates in streams (Ingold, 1975). Conidia can also be sampled from the water column by ltration or
from naturally colonized submerged substrata (e.g. leaves, twigs)

* Corresponding author.
E-mail address: sduarte@bio.uminho.pt (S. Duarte).

and substrate baits after inducing sporulation in the laboratory

(Gulis et al., 2005).
De Wildeman (1893, 1894, 1895) was the rst to recognize some
of the typical conidial forms of aquatic hyphomycetes and
described species of several genera (Clavariopsis, Lemonniera and
Tetracladium) (Fig. 1). However, these fungi only gained relevance
nearly half a century later when Ingold (1942) described 16 forms of
conidia and traced them back to mycelia on decaying alder leaves in
a stream near Leicester, in England. In the rst of many papers
devoted to aquatic hyphomycetes, Ingold (1942) wrote: My observations on aquatic hyphomycetes have been limited, so far, to
the immediate neighbourhood of Cropston in Leicestershire, but it
is of interest to know if they are of wide occurrence. In subsequent
years, he found identical or similar spores in samples from many
regions in Britain (Ingold, 1943a,b), and other parts of the world,
including Europe (e.g. Switzerland: Ingold, 1949), Africa (Nigeria:
Ingold, 1956, 1959; Uganda and Zimbabwe: Ingold, 1958;
Swaziland: Ingold, 1973), North America (Canada: Ingold, 1960) and
Caribbean Islands (e.g. Jamaica: Hudson and Ingold, 1960), thus
demonstrating the world-wide occurrence of aquatic hyphomycetes. Studies by other researchers conrmed their global distribution (e.g. California: Ranzoni, 1953; Japan: Tubaki, 1957; eastern

http://dx.doi.org/10.1016/j.funeco.2015.06.002
1754-5048/ 2015 Elsevier Ltd and The British Mycological Society. All rights reserved.

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002

S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

Fig. 1. Conidia of aquatic hyphomycetes. A, Alatospora acuminata; B, Anguillospora liformis; C, Articulospora tetracladia; D, Clavariopsis aquatica; E, Collembolispora barbata; F,
Dimorphospora foliicola; G, Dendrospora erecta; H, Flagellospora penicillioides; I, Heliscus lugdunensis; J, Heliscus submersus; K, Lemonniera aquatica; L, Lunulospora curvula; M, Tetracladium marchalianum; N, Tetracladium setigerum; O, Tetrachaetum elegans; P, Tricladium attenuatum; Q, Tricladium chaetocladium; R, Tricladium splendens; S, Varicosporium elodeae; and T, Ypsilina graminea.

USA: Petersen 1962, 1963a,b; Scandinavia: Nilsson, 1958, 1964;

South Africa: Greathead, 1961; Australia: Cowling and Waid, 1963;
Cuba: Marvanov
a and Marvan, 1969 and Malaysia: Nawawi, 1985).
Compared to other freshwater fungi, the distribution of aquatic
hyphomycetes is relatively well studied and several data compilations exist based on morphospecies (taxonomy based on morphological differences of the conidia) (e.g. Ingold, 1975; Webster and
, 1997; Santos-Flores and BetancourtDescals, 1981; Marvanova
pez, 1997; Gulis et al., 2005), although studies in tropical latiLo
tudes have been less common (e.g. Sridhar et al., 1992; Goh, 1997;
Marvanov
a, 1997). Comparable communities exist in temperate
zones on both sides of the equator; streams closer to the equator
are represented by a characteristic tropical mycoora, which
nevertheless contains many species common to temperate zones
rlocher, 1985). In fact, many species of
(Wood-Eggenschwiler and Ba

aquatic hyphomycetes have been found in stream foam collected in

different parts of the world (Ingold, 1975; Webster and Descals,
1981), suggesting that the distribution of aquatic hyphomycetes
might follow the hypothesis of Baas Becking (1934). This hypothesis
postulates, with respect to microbes, that everything is everywhere and that small organisms (<2 mm) capable of dispersal
have cosmopolitan distribution and are found in suitable habitats
with little or no evidence of historical constraints, but with the
important qualication that the environment selects (Baas
Becking, 1934). Consequently, different contemporary environments should maintain distinctive microbial assemblages (Martiny
et al., 2006).
However, questions regarding the magnitude of global species
richness, patterns of alpha (local) and beta (degree of community
differentiation) diversity and the extent of cosmopolitanism and

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
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S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

endemism of aquatic hyphomycetes remain largely unanswered.

The most convincing approach to answer these questions would be
to perform coordinated and systematic surveys in different
geographic regions, however, to our knowledge the largest study
surveyed only 4 countries over 5 latitudes and one stream per
location (Jabiol et al., 2013). Alternatively, species distribution data
from the literature can be used (e.g. Wood-Eggenschwiler and
B
arlocher, 1985; Shearer et al., 2007). In an attempt to improve
our knowledge on the geographic distribution of aquatic hyphomycetes, we gathered data on species distribution in freshwater
ecosystems from different types of substrata (natural or articial
foam, scum, water, and decaying plant litter). Studies that surveyed
aquatic hyphomycetes in terrestrial environments or temporary
aquatic ecosystems (e.g. tree holes, stem ow, rain drops, rainwater
from trees; see Chauvet et al., in this issue) were excluded. The
selected data were published between December 1942 and October
2014, and included those available in the Web of Science database, as well as others in national journals, theses and taxonomic
guides. The search terms used in the Web of Science database were:
aquatic hyphomycete or Ingoldian fungi or water borne spora
or water borne conidia or water borne fungal spores or water
borne fungal conidia or water borne fungi. Aquatic hyphomycete
species names were validated using the Index Fungorum (http://
www.indexfungorum.org/), because names of some species
changed after their rst description (up to 34 species)
(Supplementary Appendix 2). In addition, we attempted to assess
to what extent DNA-based techniques have helped to elucidate the
phylogeography of aquatic hyphomycetes, and we speculate how
recently developed molecular approaches may deepen our
knowledge in deciphering biogeographic patterns of stream
dwelling decomposer fungal communities.
2. Current knowledge of geographic distribution of aquatic
hyphomycetes
Based on data from 352 publications (Supplementary Appendix
1) documenting 335 morphospecies (Supplementary Appendix 2)
on a wide range of substrata, we conrmed that aquatic hyphomycetes are indeed very widely distributed (Fig. 2), as stated previously (Ingold, 1975; Webster and Descals, 1981; WoodEggenschwiler and B
arlocher, 1985). Not surprisingly, the most
intensively studied geographic regions include temperate zones of
the Northern hemisphere (mid-latitudes), particularly in Europe
(Fig. 2), where Ingold conducted his rst surveys (e.g. 1942,
1943a,b) followed by many other authors (Supplementary
Appendix 1). Other well-studied regions include North America
(Northern Temperate e USA and Canada), the Tropics (Venezuela,
Brazil and Puerto Rico) and Asia (Tropical Asia, in particular India)
(Fig. 2). The least studied regions are in Africa, with the exception of
South Africa, and the polar regions, where only a small number of
aquatic hyphomycetes has been reported (Fig. 2; regions dened by
the geographic location plus climate inuence as in Shearer et al.,
2007). In fact, parts of Africa have been largely neglected for
many fungal groups (Crous et al., 2006). It has been widely recognized that our perception of the geographical distribution of fungi
is inherently biased due to region-specic sampling efforts by
mycologists (Wood-Eggenschwiler and B
arlocher, 1985; Shearer
rlocher, 2010). A fundamental
et al., 2007; Raja et al., 2009; Ba
pattern in ecological studies is an increase in the number of
observed species as the sampled area increases (Zinger et al., 2014,
see next sub-section). Ecologists often use such speciesearea
curves to estimate the minimum size of a sampled area necessary to
adequately characterize a community, by plotting a curve and
estimating the area after which more sampling adds only a few
more species e the minimum area (Scheiner, 2003). We plotted a

curve with our data (Fig. 2), and used the number of studies, which
is related to the sampling effort, as a proxy of the sampled area. The
data were tted to a rectangular hyperbola (analogous to the
MichaeliseMenten equation). Based on this model, at least ca. 29
papers per region would be necessary to document 50% of the
actual number of species, and 275 papers to achieve 90% (Fig. 3). Of
the 15 geographic regions surveyed, only Northern temperate and
tropics (western hemisphere) and Europe temperate and tropical
Asia (eastern hemisphere) meet the 50% and none meets the 90%
target. Other speciesearea curves yield lower estimates (Zinger
et al., 2014), but Fig. 3 clearly suggests that for most regions,
there is only preliminary information on the true diversity of
aquatic hyphomycetes. Nevertheless, the large dataset created in
the current review allowed us to test several ecological concepts on
aquatic hyphomycetes: taxaearea and distanceedecay relationships; the inuence of latitude on species richness and of the
geographic region/climate in structuring aquatic hyphomycete
communities in world freshwaters. Since the classic indices of
compositional similarity are quite sensitive to sampling size,
especially for assemblages with numerous rare species, which was
the case of our dataset, Chao's abundance-based index was used in
all species turnover analyses (Chao et al., 2005).
2.1. Taxaearea and distanceedecay relationships
When assessing biodiversity, taxaearea and the distanceedecay
relationships are the most informative indicators of spatial turnover (Zinger et al., 2014). The former can be expressed as S k*Az,
where S corresponds to the number of species, k is a constant that is
empirically derived from the taxon and the specic location, A is the
sampled area and z the rate at which species increase with area or
the rate of species accumulation (Zinger et al., 2014). If everything
is everywhere, almost all species in a community would be expected within a very small area and few, if any new species, would
be discovered by sampling larger areas (Bell et al., 2005). For
example, Fenchel and Finlay (2004) found as many morphospecies
of protists in a single lake as previously described from the entire
world. Earlier studies suggested that z for microbial taxa (ca.
0.002e0.07) falls well below that observed for taxonomic groups of
larger organisms (ca. 0.1e0.6) (Bell et al., 2005; Zinger et al., 2014).
However, more recent evidence suggests that the rate of species
increase observed for plants and animals may also be found for
certain microbes (ca. 0.3e0.6) (e.g. ectomycorrhizal fungi, Peay
et al., 2007; marine bacteria, Zinger et al., 2014). By using the
number of studies, which is related to the sampling effort, as a
proxy of the sampled area, at a regional scale (70 regions that
corresponded to different countries except for USA, Canada and
Russia where 3 regions were dened), we calculated a z of 0.6923
(Fig. 4A), which is quite similar to that found for communities of
larger organisms (e.g. Bell et al., 2005). However, we are not able to
conclude that some aquatic hyphomycetes have a restricted
geographic distribution, due in part to the uneven number of
studies conducted in different regions. In addition, some of these
studies were conducted many years or decades apart, which may
bias our analysis. For instance, most of the data obtained for the
African continent rely on very old studies and many aquatic
hyphomycetes were not identiable to species at that time (e.g.
Ingold, 1956, 1958, 1973).
Recently, Sato et al. (2012) hypothesized that the biogeographic
distribution of microbial species depends on their colonization
ability and degree of isolation of suitable habitats; species that
experience negligible constraints for colonization may have
broader distribution (e.g. root-inhabiting fungi with low host
specialization) (Queloz et al., 2011) than those with strong colonization constraints (e.g. host specicity) and habitat isolation (e.g.

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
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Eastern Hemisphere

400

sub-Arctic
Boreal
Temperate

300

Tropical
sub-Tropical

200
100

Oceania

Tropical Asia

Temperate Asia

Temperate Africa

Tropical Africa

Northern Africa

Mid East

Europe temperate

Boreal

sub-Arctic

Southern Temperate

Tropics

Northern Temperate

Boreal

sub-Arctic

Aquatic hyphomycete
species richness

Western Hemisphere

Fig. 2. Distribution of aquatic hyphomycetes (335 species) and species richness in 15 geographic regions in the western and eastern hemispheres (dened based on the geographic
location plus climate inuence; Shearer et al., 2007). Data were retrieved from 352 diversity surveys based on morphospecies (i.e., morphological differences in fungal conidia).
Different colours depict different climatic inuences and bicolour dots are climatically intermediate locations. Details on the surveys are in Supplementary Appendix 1.

ectomycorrhizal fungi: Sato et al., 2012; Tedersoo et al., 2014a,b;

hot-spring cyanobacteria: Papke et al., 2003; Whitaker et al., 2003).
The wide geographic distribution of aquatic hyphomycetes sugrlocher, 2009), which would
gests excellent dispersal abilities (Ba
tend to atten the relationship between species richness and
rlocher, 2010). Although the diversity of aquatic
sampled area (Ba
hyphomycetes is high in pristine habitats (Krauss et al., 2011), some
species are remarkably resilient and can occur in harsh environments, such as in streams with high levels of metals (Krauss et al.,
 et al., 2008), and/or high nutrient loads (Pascoal and
2001; Sole
C
assio, 2004; Pascoal et al., 2005; Duarte et al., 2009), and even
in sulphur springs with temperatures reaching 36.5  C

(Chandrashekar et al., 1991). Constraints due to substratum specicity should also be less stringent, since most aquatic hyphomycetes are capable of colonizing a wide range of deciduous leaves
(Webster and Descals, 1981), though substrata such as wood and
grass appear to be more selective (Gulis, 2001). On the other hand,
streams within the same region but with different physicochemical conditions harbour different communities (e.g. Pascoal
 et al., 2008; Duarte et al.,
et al., 2005; Castela et al., 2008; Sole
2009). This suggests a degree of selective colonization and niche
differentiation by aquatic hyphomycetes.
The distanceedecay relationship indicates how similarity in
community composition changes with geographic distance

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
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S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

Species richness S

400
300
200
100

SE)

r = 0.9252

limiting the dispersal of aquatic fungi (there are several species

with cosmopolitan distribution, i.e. identical species occur in
different continents and in geologically young islands), but that
their community structure is strongly inuenced by complex biotic
and abiotic factors determined on a regional basis (Woodrlocher, 1983).
Eggenschwiler and Ba
Therefore, a global scale analysis with substantial sampling
effort is needed to elucidate the relative inuence of contemporary
and seasonally uctuating environmental factors versus the legacies of historical events/natural barriers on present-day distribution patterns of aquatic hyphomycetes.

0
0

50

100

150

200

Sampling effort SE
Fig. 3. Relationship between aquatic hyphomycete species richness and the sampled
area. The number of studies, which is related to the sampling effort, was used as a
proxy of the sampled area for each geographic region (see Fig. 2). Data were tted to
the MichaeliseMenten model in Prism 4.0 for Windows (GraphPad software Inc., San
Diego, CA, USA).

between sites, and represents the compositional turnover rate

(Green et al., 2004), and any effect of richness (e.g. Legendre, 2014).
We found that aquatic hyphomycete community similarity based
on morphospecies negatively correlated with increasing
geographic distance (Fig. 4B). However, the dispersion of our data
was high (r2 0.065), in part because conidial abundance in
streams is strongly affected by natural or anthropogenic factors,
which can uctuate on a daily or seasonal scale. These factors
rlocher et al., 2011), pH
include temperature (e.g. Chauvet, 1991; Ba
(e.g. B
arlocher and Rosset, 1981; Casas and Descals, 1997), conductivity (e.g. Wood-Eggenschwiler and B
arlocher, 1983), altitude
rlocher et al., 2011), differences in riparian
(e.g. Chauvet, 1991; Ba
rlocher and Graa, 2002), and presence of various
vegetation (Ba
 et al., 2008; high nutrient loads, Pascoal
pollutants (e.g. metals, Sole
et al., 2005; Castela et al., 2008; Duarte et al., 2009; SchoenleinCrusius et al., 2009). These confounding factors might blur overall
patterns of aquatic hyphomycete diversity distribution. In bacteria,
the relative inuence of historical (natural barriers) versus environmental factors seems to be related to the scale of sampling
(Martiny et al., 2006). Communities separated by only a few kilometres (up to 10 km) were structured by environmental factors
(Kuske et al., 2002; Horner-Devine et al., 2004), while at intermediate scales (10e3000 km), signicant effects of distance were
detected (Green et al., 2004; Reche et al., 2005; Yannarell and
Triplett, 2005). On the other hand, at an intercontinental scale,
bacterial assemblages in hot springs were differentiated by distance but did not correlate with any environmental variable (Papke
et al., 2003; Whitaker et al., 2003). A similar pattern was found for
fungi from wetland sediments in China; variation in fungal diversity was driven by natural barriers at a regional sale
(1000e4000 km) and by environmental factors at a smaller scale
(<1000 km) (Wu et al., 2013). In fact, environmental factors inuence the composition of aquatic hyphomycete communities at
small spatial scales (2.9e100 km) (Pascoal et al., 2005; Castela et al.,
 et al., 2008; Duarte et al., 2009). In 16 streams distrib2008; Sole
uted by 4 geographic areas in France, Germany and Switzerland,
community similarity was highest within each region and clear
differences between regions were found (Wood-Eggenschwiler and
B
arlocher, 1983). But in Australian streams, separated by up to
175.7 km, the distance between streams accounted for a small
portion of the variability, while altitude, followed by temperature
had the most pronounced impact (B
arlocher et al., 2011). Thus,
previous studies suggested that there are few geographical barriers

2.2. Latitude and climatic inuence

An increase in species richness from higher (polar zones) towards lower latitudes (equatorial zones) is the oldest and most
fundamental pattern of the distribution of life on earth and a widely
documented macroecological pattern, in particular in terrestrial
ecosystems (e.g. Rosenzweig, 1995). In our study, aquatic hyphomycete diversity was lowest at latitudinal extremes and peaked at
mid-latitude regions (temperate streams) (Figs. 2 and 4C), as found
rlocher, 1985;
in previous surveys (Wood-Eggenschwiler and Ba
Shearer et al., 2007; Jabiol et al., 2013), but diverging from the
conventional macroecological pattern with higher diversity in the
tropics. The latter was conrmed in a recent study on freshwater
lignicolous fungi (Hyde et al., 2015). Shearer et al. (2015) examined
the distribution of freshwater ascomycetes along an elevational
gradient (as analogue of latitudinal gradient) in Peru from the
Andes to the Amazon lowlands. They found a slight peak at midelevations, however, in addition to altitude, pH had a strong effect on fungal communities. Shearer et al. (2015) did not specify the
stream order of their collection sites; regardless of altitude, many
physico-chemical and biotic properties change in a more or less
predictable manner as one moves downstream (Vannote et al.,
1980).
If real, the greater diversity of aquatic hyphomycetes in
temperate streams may be explained by season due to more
diversied ecological niches (Shearer et al., 2007; Jabiol et al.,
2013). Graa et al. (2015) hypothesized that lower turbulence and
nutrient concentrations in many of the examined tropical/subtropical streams and the presence of more highly defended leaves
may have contributed to the lower diversity of aquatic
hyphomycetes.
Kennedy et al. (2012) recently hypothesized that diversication
of ectomycorrhizal fungi may be more rapid in temperate than
tropical habitats, but at a global scale the latitudinal patterns of
diversity of soil fungi were similar to those of plants and animals e
a decrease was found towards the poles (Meiser et al., 2014;
Tedersoo et al., 2014b).
Aquatic hyphomycete community similarity decreased with the
increase of latitudinal difference (Fig. 4D). This lends some
credence to Ingold's (1966) statement I think I could tell my latitude with an error of 15 by examining the aquatic spores in a
sample of stream foam, and emphasizes the impact of latitude on
the distribution of aquatic hyphomycetes. Non-metric multidimensional scaling analysis (MDS) based on the occurrence of the
335 aquatic hyphomycete species in 15 geographic regions (denition based on the geographic location plus climate inuence;
Shearer et al., 2007) (Figs. 2 and 5, Supplementary Appendix 2)
suggests higher similarities between geographically distant locations with similar climate (e.g. Tropical Asia and South America or
Temperate Europe and North America or Temperate Asia and
Temperate Africa). Wood-Eggenschwiler and B
arlocher (1985)
reached similar conclusions based on the distribution of over 150
aquatic hyphomycete species.

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Species richness S
(log)

Community similarity CS

2
logS = 0.6923*logSEf + 2.739
2
0.5514

1.0

0.8
0.6
0.4
0.2
0

Species richness S

200 S = 64.71/(1+((L-41.26)/
150

(-36.89)) )
r = 0.08394

100
50

1.0

0.8

CS = -2.042*10 *L + 0.4397
r = 0.06457
P<0.0001

0.6
0.4
0.2
0

-90-75-60-45-30-15 0 15 30 45 60 75 90

Latitude L ()

50

100

150

Pairwise latitudinal difference L ()

60

20

Endemic species
richness SE

25

5000 10000 15000 20000 25000

Geographic distance (km) GD

Community similarity CS

Sampling effort SEf (log)

Cosmopolitan species
richness SC

CS = -1.183*10 *GD + 0.4687

r = 0.06530
P<0.0001

SE = 2.046*exp
r = 0.8112

40

15
10

0.02076*S

20

SC = (27.34*S)/(30.18+S)
r = 0.7555

0
0

50

100

150

200

0
0

50

100

150

200

Species richness S
Fig. 4. Relationships between: sampling effort (SEf) (number of studies) and species richness (S) (in 70 regions) (A), geographic distance (GD) and community similarity (CS) (B),
latitude (L) and species richness (C), pairwise latitudinal difference and community similarity (D), species richness and cosmopolitan species (SC) (E), and species richness and
endemic species (SE) (F). Linear regression models gave best ts for the relationships in (A), (B) and (D). Non-linear regression models gave best ts for the relationships in (C)
(Lorentzian model), (E) (MichaeliseMenten model), and (F) (exponential model). Similarity analysis of aquatic hyphomycete communities in (B) and (D) were assessed with Chao's
abundance-based Srensen index in EstimateS 9.0 for Windows (Colwell, 2013). The incidence of each species was based on the number of times it appeared in the 352 publications
surveyed. Regression analyses were performed in Prism 4.0 for Windows (GraphPad software Inc., San Diego, CA, USA).

In our study, 4 species occurred in all 15 geographic regions

(Alatospora acuminata, Anguillospora longissima, Articulospora tetracladia and Lemonniera aquatica), 36 species occurred in 10 of the
geographic regions (Appendix 2), and 67 species were restricted to
1 geographic region. Aquatic hyphomycetes may follow a biogeographical model of restricted moderate endemism, as suggested by
Foissner (1999) for small eukaryotes; some species are cosmopolitan whereas others are biogeographically and ecologically limited.
Jabiol et al. (2013) in a recent survey across a broad latitudinal
gradient also found many species with cosmopolitan distribution
from the arctic to the tropics (e.g. A. tetracladia, Flagellospora curvula), while others were restricted to single locations (e.g. Triscelophorus acuminatus and Triscelophorus monosporus were only
observed in the tropical location). One of the major constraints of
aquatic hyphomycete diversity analysis based on morphospecies is

that the probability of nding rare species depends on the approach

used to document the occurrence of conidia. The simultaneous use
of several methods e collection of natural foam and plant substrata,
and the use of articial foam and substratum baits e will increase
the probability of nding rare species (e.g. Shearer and Webster,
1985; Pascoal et al., 2005). In fact, while the number of cosmopolitan species (found in more than 50% of the regions) increased
asymptotically with the total number of species found at a regional
scale (Fig. 4E), the number of endemic or rare (found in less than
10% of the regions) species increased exponentially (Fig. 4F). Species that are present but not captured lead to undersampling or
unequal sampling and are one of the major sources of error when
estimating microbial diversity (Torsvik et al., 2002; Sato et al.,
2012). Our understanding of the geographical distribution of
aquatic hyphomycete species would clearly benet from more

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002

S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

1.5

2D Stress: 0.1
Tropical
sub-Tropical
Temperate
Boreal
sub-Arctic

1.0
0.5 15 12 14

1
7

-3.0

-2.0

6
-1.0

13

11
1.0

2.0

3.0

-0.5
10

-1.0
5

-1.5

Fig. 5. Non-metric multi-dimensional scaling (MDS) ordination diagram based on aquatic hyphomycete communities in each geographic region (dened by geographic location
plus climate inuence; Shearer et al., 2007). Similarities of aquatic hyphomycete communities were assessed with Chao's abundance-based Srensen index in EstimateS 9.0 for
Windows (Colwell, 2013). The incidence of each species was based on the number of times it appeared in the 352 publications surveyed. Western hemisphere: 1, sub-Arctic; 2,
Boreal; 3, Northern temperate; 4, Tropics; 5, Southern temperate; Eastern hemisphere: 6, sub-Arctic; 7, Boreal; 8, Europe temperate; 9, Mid East; 10, Northern Africa; 11, Tropical
Africa; 12, Temperate Africa; 13, Temperate Asia; 14, Tropical Asia and 15, Oceania. Different colours depict different climatic inuences and bicolour dots are climatically intermediate locations. MDS analysis was performed in Primer v6 for Windows (Plymouth, UK).

comprehensive sampling strategies that can capture a higher

diversity.
2.3. Contribution of DNA-based studies to reveal phylogeographic
patterns
Since most aquatic hyphomycete species are believed to be
readily identiable by their conidial morphology, ecological studies
continue to rely on this straightforward approach to measure
fungal diversity (Gulis et al., 2005) (Fig. 1). Partly for this reason,
DNA based techniques were applied later to aquatic hyphomycetes
than to other morphologically less diverse fungal groups (e.g.
Nikolcheva et al., 2003; Manerkar et al., 2008; Seena et al., 2008;
Clivot et al., 2013). Using the reproductive ability of a fungus as a
proxy for its contribution to ecological functions or overall diversity, presents a clear bias in favour of prolic spore producers
(e.g. Duarte et al., 2009). In addition, accurate identication is often
difcult or impossible in species producing less differentiated
conidia (e.g. scolecoid conidia). Many aquatic hyphomycete species
appear to be cosmopolitan, but conclusions based on morphospecies overlook cryptic species and may blur global-scale biogeographical patterns. Indeed, DNA-based studies in other fungal
groups are providing increasing evidence that not everything is
everywhere and that fungi do have a biogeography (Hibbet, 2001;
Dettman et al., 2006; Taylor et al., 2006; Meiser et al., 2014).
At present, molecular studies on the phylogeography of aquatic
hyphomycetes do not allow any well-supported conclusions, since
very few attempts have been made to analyse biogeographic patterns based on DNA data. Two studies using internal transcribed
spacer region (ITS) barcodes from cosmopolitan species with isolates from different geographic regions, have somewhat contradictory conclusions (Duarte et al., 2012; Seena et al., 2012). Several
ITS genotypes of A. tetracladia were geographically widespread
(Iberian Peninsula, Central Europe, United Kingdom, Canada, and
Japan) irrespective of sampling time, substratum or location (Seena
et al., 2012), but Malaysian genotypes grouped in a different

phylogenetic clade and were not shared by other countries (Seena

et al., 2012). Duarte et al. (2012) studied ITS genotypes of 130
strains from 6 species isolated from plant litter or foam in streams
in Europe and Australia. Distribution patterns were speciesspecic: European and Australian genotypes of Anguillospora liformis, Flagellospora penicillioides, Geniculospora grandis and Tetrachaetum elegans were consistently different, while those of
Lunulospora curvula and Tricladium chaetocladium were intermixed
in the phylogenetic trees. Similar genotypes were found in both
continents for T. chaetocladium, suggesting intercontinental gene
ow in this species (Duarte et al., 2012).
On the other hand, a study with 97 isolates of T. elegans from 9
streams within a 1450 km2 area in Southwestern France showed
that only 20% of molecular variance, assessed by amplied fragment length polymorphism (AFLP), was explained by stream location (Laitung et al., 2004). Although a high genotypic diversity
based on polymorphic microsatellite loci was found for 391 isolates
of Tetracladium marchalianum from rivers in Illinois and Wisconsin
(Anderson and Shearer, 2011), stable genetic differentiation was
only observed between the most distant rivers (ca. 450 km)
(Anderson and Shearer, 2011). These studies suggest that environmental barriers to dispersal may play a role in the genetic structure
of aquatic hyphomycete species, but patterns were not consistent
and biogeography within aquatic hyphomycetes may be speciesspecic. In addition, the analysis of 96 strains of T. elegans from a
single site yielded 13 random amplied polymorphic DNA (RAPD)
proles and some genotypes were more abundant on particular leaf
species and rare or absent in others (Charcosset and Gardes, 1999).
Thus, the resource quality (substrate type) may constrain aquatic
hyphomycete colonization.
Unfortunately, the sample size of most studies was small
(number of isolates or spatial scale) and relied on DNA from pure
cultures. This conventional approach is time-consuming and its
success is greatly affected by the probability of getting isolates from
different geographic areas belonging to the same morphospecies
(Duarte et al., 2012). Phylogenetic information for many lineages,

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002

S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

their abundances and geographical occurrence, and the associated

environmental data are clearly needed to elucidate why populations of a given aquatic hyphomycete (morpho)species occur
rlocher,
and persist in a geographic region, but not in others (Ba
2010).
3. Do molecular tools promise a deeper knowledge in
deciphering the biogeography of aquatic hyphomycetes?
Molecular tools have dramatically increased our knowledge of
Fungi in less than 20 years (Persoh, 2015), but many fungal species
remain to be discovered (Blackwell, 2011). There is no doubt that
molecular techniques provide powerful tools to reveal streamdwelling fungal diversity more deeply and widely than ever
rlocher, 2010, in this issue). Understanding the biogeogbefore (Ba
raphy of aquatic fungi will continue to benet from these methodological advances.
Different molecular tools have been applied to assess streamdwelling decomposer fungal communities (DGGE: 5 streams in
Northwestern Portugal, Duarte et al., 2009; 5 streams in Northeastern France, Clivot et al., 2013; 9 streams in South-central
Sweden, Bergfur and Sundberg, 2014; clone libraries: 5 streams in
Northeastern France, Clivot et al., 2013; and 454 pyrosequencing:
30 streams in North-western and -eastern Finland, Tolkkinen et al.,
2013; Heino et al., 2014; 5 streams in Northwestern Portugal,
Duarte et al., 2015). In these studies, aquatic hyphomycete communities were structured by similar environmental drivers,
regardless of whether they were evaluated by conidium identication or genetic diversity (e.g. pH, nutrients, uvial geomorphology) (Duarte et al., 2009; Clivot et al., 2013; Bergfur and
Sundberg, 2014; Duarte et al., 2015). But studies relying on 454
pyrosequencing detected differences at the genetic level; for
instance, A. tetracladia operational taxonomic units (OTUs) on
decomposing oak leaves differed among streams along a gradient of
eutrophication (Duarte et al., 2015). In fact, intraspecic traits of
A. tetracladia modulated the effects of biodiversity on ecological
processes (e.g. plant litter decomposition) under stress conditions
(Fernandes et al., 2011). Next generation sequencing technology
promises a higher resolution for testing the degree of differentiation between communities.
An additional advantage of pyrosequencing is its sensitivity to
detect very rare species recovered as singletons i.e., unique sequences that may be informative of exclusive lineages in rare
biospheres (Zhan et al., 2013). Rare taxa may contribute disproportionally to overall metabolic activities (Jones and Lennon,
2010; Campbell et al., 2011), carry out unusual metabolic functions (Galand et al., 2009) and show distinct spatial distribution
patterns. Applying Next Generation Sequencing (NGS) to cDNA (the
synthesis of cDNA from RNA is only possible in metabolically active
species) (e.g. Kuramae et al., 2013) will provide greater insights into
metabolically active species.
To disentangle the relative importance of local versus regional
factors in structuring aquatic hyphomycete communities in world
freshwaters, repeated, multi-scale sampling is crucial (Heino et al.,
2014). In fact, the pyrosequencing of soil samples from 365 globally
distributed sites allowed, for the rst time, integrating fungi into a
general macroecological framework (Tedersoo et al., 2014b). Environmental parameters weakly explained community composition
of plant-associated fungi (endophytic, root-associated and soil),
and effects were inconsistent at local and regional scales in meta'omics studies (Persoh, 2015). But decreased community similarity
with increasing distance from local to global scales seems to be due
to the inability of fungi to establish themselves at a particular locality (i.e. via environmental ltering or competitive exclusion),
rather than to spatially limited dispersal (Persoh, 2015). This is in

accordance with a meta-analysis of fungal communities from

phyllosphere and soils based on 454 pyrosequencing suggesting
that globally distributed OTUs may be rare in fungi (Meiser et al.,
2014). In fact, only 14% of the fungal species overlapped in soil
samples collected at a distance of 1 m (Taylor et al., 2010). Similar
results were found in pyrosequencing studies of other microbial
eukaryotic communities from the deep-sea (fungi, nematodes,
protists) (Bik et al., 2012; Creer and Sinniger, 2012) and protozoa
from soil, freshwater and marine sediments (Bass et al., 2007). A
few taxa were cosmopolitan, but the majority showed restricted
and/or patchy distribution.
NGS technologies will continue to improve both accuracy and
throughput and, in the near future, benchtop sequencers will
become standard equipment in individual labs. Amplicon analyses
are expected to become a rapid screening technique in preparation
for more detailed metagenomic studies, rather than representing
the nal stage in ecological analysis (Nikolaki and Tsiamis, 2013).
While NGS technologies may inform us that different geographic
regions harbour different aquatic fungal communities, they will not
reveal much about their function. This will require the application
of functional metagenomics, i.e. analysis of the complete genetic
information including the relative abundance of all genes, allowing
a description of the functional potential of each community
(Chistoserdova, 2014). Coupling metagenomic analyses with
extensive cross-site sampling efforts led to a more comprehensive
picture of biogeographical patterns in diversity, community
composition and functional attributes of soil fungal communities
(Fierer et al., 2012). New approaches exploiting NGS technologies
and single cell genomics (characterizing genomes of uncultured
phyla from single cells obtained directly from the environment;
Lasken, 2007) may target genomes and associate them with
quantitative measurements in particular geographic regions. This
approach potentially targets all active members (abundant and
rare) of a given ecosystem, quanties the transcribed genes, and
obtains complete genomes (Nikolaki and Tsiamis, 2013). Single cell
genomics have been employed to investigate the biogeographic
distribution of uncultured marine Flavobacteria and marine bacterioplankton (Mason et al., 2012; Woyke et al., 2009). The application of this methodology to stream-dwelling decomposer fungi
seems feasible because a single spore can be used as a source of
rlocher et al., 2010).
DNA (Ba
Outlook and perspectives
A central question in ecological research is how biodiversity is
structured by spatial processes and environmental factors. The
conventional view in microbial ecology emphasized that everything is everywhere, but the environment selects (Baas Becking,
1934), implying that microbial species occur at sites of suitable
conditions instead of occurring at specic geographic locations. It
has been assumed that aquatic hyphomycetes have a world-wide
,
distribution (e.g. Ingold, 1975; Sridhar et al., 1992; Marvanova
1997), but relevant information is still scarce partly due to uneven sampling efforts in different geographic regions (Jabiol et al.,
2013). In addition, most surveys have been based on the
morphology of detached conidia, which can be ineffective or
misleading when dealing with closely related or morphologically
convergent species. DNA-based studies might avoid the pitfalls
presented by studies based on morphospecies. Recent sequencing
efforts are revealing a large amount of hidden microbial diversity
(e.g. Meiser et al., 2014). However, many ecosystems, among them
streams, where aquatic hyphomycetes play a key role in organic
matter turnover, remain largely unexplored (but see Duarte et al.,
2015) and are promising targets for discovering new fungal taxa
and revealing diversity patterns. High-throughput studies have

Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002

S. Duarte et al. / Fungal Ecology xxx (2015) 1e10

barely scratched the surface of the vast information that remains to

be explored concerning stream-dwelling decomposer fungi. As
more locations are scrutinized and sequencing efforts become more
extensive with new technology, more endemic species may be
discovered. More studies, incorporating different habitats and
environmental conditions, are needed to decipher global trends of
fungal biodiversity in world freshwaters, and metagenomic approaches that use a combination of taxonomic, phylogenetic and
functional diversity applied in coordinated surveys at a global scale
will be indispensable for revealing these patterns.
Acknowledgements
This work was supported by FCT I.P. through the strategic
funding UID/BIA/04050/2013. Financial support granted by the FCT
to S. Duarte (postdoctoral fellowship SFRH/BPD/47574/2008) is also
gratefully acknowledged.
Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.funeco.2015.06.002.
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Please cite this article in press as: Duarte, S., et al., Biogeography of aquatic hyphomycetes: Current knowledge and future perspectives, Fungal
Ecology (2015), http://dx.doi.org/10.1016/j.funeco.2015.06.002