Animal Welfare

ANIMAL SCIENCE, ISSUES AND RESEARCH
ANIMAL WELFARE
ASSESSMENT, CHALLENGES AND
IMPROVEMENT STRATEGIES
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ANIMAL SCIENCE, ISSUES
AND RESEARCH
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ANIMAL SCIENCE, ISSUES AND RESEARCH
ANIMAL WELFARE
ASSESSMENT, CHALLENGES AND
IMPROVEMENT STRATEGIES
JEREMIAH WEAVER
EDITOR
New York
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CONTENTS
Preface vii
Chapter 1 The Roles of Time and Space in Zoo
Animal Welfare 1
Stephanie M. Allard, Grace A. Fuller
and Jennifer L. Hamilton
Chapter 2 An Integrative Approach to Realizing Animal
Welfare - Ethics, Environment and Science 55
Ryunosuke Kikuchi,
Rosário Plácido Roberto da Costa and
Myriam Kanoun-Boulé
Chapter 3 Bestiality and the Law:
A Form of Animal Protection or Protection
of Public Morals? A Need for Reform-Animals
as Victims of Sexual Abuse 87
Laura Donnellan
Chapter 4 Animal Welfare in the European Union’s
External Relations Law 125
Yumiko Nakanishi
Chapter 5 Moving in the Right Direction: Painful Husbandry
Procedures Tend to Be a Thing of the Past 147
Agustín Orihuela
Index 157
PREFACE
Animal welfare science has advanced greatly in the last several decades.
This trend is also evident in the zoo and aquarium community, where
resources are increasingly being dedicated to better understanding how
captivity impacts animals and how best to assess and improve the welfare of
individual animals living in the care of humans. In this book, Chapter One
examines how far the zoo community has come in addressing the welfare
needs of animals in varying housing conditions and highlights areas in need of
further attention and research. Chapter Two discusses animal welfare from the
viewpoints of cruelty, conservation of wild animals and veterinary attention.
Chapter Three examines the justifications for the criminalisation of bestiality
and argues that bestiality should be placed within the confines of animal
welfare legislation and the focus should be on the animal and respecting the
animal and its need to be able to exhibit normal behaviour patterns and its
need to be protected from sexual abuse. Chapter Four analyzes from a legal
perspective the European Union’s (EU) measures and strategies for animal
welfare in its external relations and highlights the development of the concept
of animal welfare in the EU and in its relationships with the rest of the world.
Chapter Five studies the growing demand for healthier animal products and
the improvement of animal well-being.
Chapter 1 - Decades of research and systematic management have
enhanced the knowledge and capacity to create zoo habitats that provide
animals with opportunities to express natural behaviors, make choices, and
exert control over aspects of their environments. As the understanding of
animal welfare has grown, so has the realization that positive welfare must be
promoted 24 hours a day, 365 days a year, and throughout an animal’s entire
life. Zoo animals reside in spaces that may vary depending on time of day and
viii Jeremiah Weaver
time of year. In some cases, this can create challenges when it comes to
assessing and improving individual animal welfare. Considering individual
responses to variation in housing, and assessing the benefits of various night-
time housing conditions is key if zoos are going to move beyond the more
traditional practice of bringing animals into holding areas at night. Here the
authors examine two case studies highlighting the challenges and opportunities
for assessing welfare outside of traditional times and spaces. Using keeper
ratings along with non-invasive measures of adrenal activity, the authors
compared the effects of overnight access to an indoor habitat to more
traditional night holding spaces for gorillas and drill monkeys. Keeper ratings
are becoming more widely used as a measure of wellbeing, and the authors
also discuss some of the challenges associated with this methodology. Second,
the authors monitored four aardvarks using infrared video to assess how
occupying different night spaces impacted behavioral and hormonal measures
of their welfare. Nocturnal animals are active during time periods when zoo
personnel are not typically present both to observe the individuals and to
provide them with additional behavioral opportunities. Understanding how
individuals utilize their space and partition their time overnight can help to
ensure their needs are met even when staff members are not present. Through
the exploration of these case studies, the authors the authors examine how far
the zoo community has come in addressing the welfare needs of animals in
varying housing conditions and highlight areas in need of further attention and
research.
Chapter 2 - Animal welfare has become an important issue in recent years.
There is an increasing interest in animal welfare in many countries.
Urbanization, the influence of the media and civil society organizations, and
higher levels of education are reasons for an increased interest in animal
welfare. Consideration of animal welfare should encompass not only the
physical health but also the psychological well-being of animals. The term
‘welfare’ defines the state in which a person or animal lives healthily, happily
and safely. The subject of animal welfare is discussed from the viewpoints of
cruelty (ethics), conservation of wild animals (environment) and veterinary
attention (science). The majority of people believe that animals are currently
raised without cruel treatment, but reports of animal cruelty are not unknown:
for example, bear farming typically entails the imprisonment of bears in
squeeze cages for years; a catheter is inserted daily into a bear’s gall bladder or
a tube is implanted internally in order to collect dripped bile; workers often
mutilate the bears by breaking their teeth and pulling out claws for the sake of
human safety; and when the bears cannot produce sufficient bile, they are left
Preface ix
to die of starvation or are killed for their parts. Habitat loss, climate change,
poaching, and pollution paint a bleak picture for threatened and endangered
species around the world. It is estimated that about 10,000 species annually
become extinct. This rapid extinction is happening through the trade in at-risk
species, expanding cities which destroy habitats, the conversion of fertile
wildlife land habitat for agriculture or pastures and human-driven changes.
Directly or indirectly, human society has multiple impacts on wild animals’
welfare and survival. Natural reserves, protected areas and rehabilitation
centers for threatened wildlife are some of the possible ways to counterbalance
our footprint on wild fauna and to promote protection and conservation.
However, if international policies are essential for starting and moving
towards a standard concept of animal welfare, effective realization of this
concept can be achieved only through keen environmental awareness by
citizens around the globe. The veterinary profession is privileged to occupy a
position of enormous social influence on animal welfare issues. However, the
profession has traditionally understood welfare primarily within the limited
scope of animal health and productivity. Currently, animal welfare focuses on
companion and farm animals, and welfare during transport of the animals and
at slaughter, but a greater emphasis must be placed on the welfare of wild
animals in captivity or conservational parks and those animals that have lost
their natural habitats. The importance of animal welfare differs from country
to country owing to differences in religion, economic development, education
and perception. Animal welfare is not restricted to a single field: it is a subject
that interests both scientists and the public. Although it is not enough to
discuss only one aspect of animal welfare, an integrative approach is may be
necessary to describe the concept of animal welfare.
Chapter 3 - Bestiality is a topic that evokes much revulsion and disdain. In
jurisdictions where bestiality is a criminal offence, the legislation has as its
focus the protection of public morals. It is seen as an abasement of the person.
At common law, the offence was enveloped in religious terms, words such as
“unnatural” and “abominable” were used to highlight the perceived immoral
nature of the crime. Bestiality was juxtaposed with sodomy; both were viewed
as moral equivalents that had no place in polite society. Those that engaged in
either act faced execution. Over time societal attitudes towards homosexuality
changed, however, bestiality remains a heinous offence. The criminalisation of
bestiality has nothing to do with animal welfare. The fate of the animal is of
little concern to the legislature. The laws are drafted from anthropocentric
context; the offender in some ways becomes the victim as they are often
viewed as psychologically unwell and in need of treatment. Bestiality is also
x Jeremiah Weaver
viewed as a gate way crime, one that leads offenders to sexually abuse
children and vulnerable adults. Animals are used for many purposes from food
to clothing to entertainment and thus not seen as having an existence outside
the needs of humans. Humans have dominion over animals and so long as the
animal does not suffer unnecessarily, the law does not intrude. While
legislation may purport to protect animals from unnecessary harm and
suffering, the proprietary status of animals permits harm so long as it is not
gratuitous and constitutes good reason. Why should bestiality be singled out?
This chapter will examine the justifications for the criminalisation of bestiality
and will argue that bestiality should be placed within the confines of animal
welfare legislation and the focus should be on the animal and respecting the
need to be protected from sexual abuse.
Chapter 4 - Animal welfare is an important issue in European Union (EU)
Article 13’s Treaty on the Functioning of the European Union (TFEU). The
EU has taken measures toward animal welfare. Some of those measures have
influenced third countries or have been criticized by other countries. For
example, an EU measure banning seal product imports became a point of
conflict between the EU and Canada in the World Trade Organization (WTO).
On the other hand, the EU has concluded and is negotiating free trade
agreements (FTAs) with third countries. Animal welfare is regulated in those
agreements, based on input from civil societies and non-governmental
organizations (NGOs). This article aims to analyze from a legal perspective
the EU’s measures and strategies for animal welfare in its external relations
and to highlight the development of the concept of animal welfare in the EU
and in its relationships with the rest of the world.
Chapter 5 - Early painful husbandry practices that were standard
procedures in animal production some years ago, have almost become obsolet.
Examples of these practices include: the trimming of beaks, toes, combs or
wattlers and the production of capons on birds; penis deviation, reduction of
the preputial orifice, blocking of the sigmoidal flexure, electroeyaculation and
dehorning on ruminants; the use of nose rings and sugical castration on pigs;
branding and lip tattoo on horses and mulesing on sheep. Most of these
procedures have been substituted for more eficient and painless alternatives. In
addition, for those painful procedures that continue to be applied, several pain
control protocols have been developed based on the use of different
combinations of sedatives, anestethics and analgesics, particularly using the
last generation of nonsteroidal anti-inflammatory drugs to minimize pain when
animals are subjected to such practices. It can not be denied the importance
Preface xi
that a more participative society involved in how farm animals are raised, a
growing demand for healthier animal products and the cummulative scientific
results of a developing animal welfare sciene have had in the significant
improvement of the animal wellbeing.
In: Animal Welfare ISBN: 978-1-53610-293-2
Editor: Jeremiah Weaver © 2016 Nova Science Publishers, Inc.
Chapter 1
THE ROLES OF TIME AND SPACE IN

ZOO ANIMAL WELFARE
Stephanie M. Allard , PhD, Grace A. Fuller, PhD

*
and Jennifer L. Hamilton

Center for Zoo Animal Welfare, Detroit Zoological Society,
Royal Oak, MI, US
ABSTRACT
Decades of research and systematic management have enhanced the
knowledge and capacity to create zoo habitats that provide animals with
opportunities to express natural behaviors, make choices, and exert
control over aspects of their environments. As the understanding of
animal welfare has grown, so has the realization that positive welfare
must be promoted 24 hours a day, 365 days a year, and throughout an
animal’s entire life. Zoo animals reside in spaces that may vary
depending on time of day and time of year. In some cases, this can create
challenges when it comes to assessing and improving individual animal
welfare. Considering individual responses to variation in housing, and
assessing the benefits of various night-time housing conditions is key if
zoos are going to move beyond the more traditional practice of bringing
animals into holding areas at night. Here we examine two case studies
highlighting the challenges and opportunities for assessing welfare
outside of traditional times and spaces. Using keeper ratings along with
non-invasive measures of adrenal activity, we compared the effects of
*
Corresponding Author: sallard@dzs.org.
2 Stephanie M. Allard, Grace A. Fuller and Jennifer L. Hamilton
overnight access to an indoor habitat to more traditional night holding

spaces for gorillas and drill monkeys. Keeper ratings are becoming more
widely used as a measure of wellbeing, and we also discuss some of the
challenges associated with this methodology. Second, we monitored four
aardvarks using infrared video to assess how occupying different night
spaces impacted behavioral and hormonal measures of their welfare.
Nocturnal animals are active during time periods when zoo personnel are
not typically present both to observe the individuals and to provide them
with additional behavioral opportunities. Understanding how individuals
utilize their space and partition their time overnight can help to ensure
their needs are met even when staff members are not present. Through the
exploration of these case studies, we examine how far the zoo community
has come in addressing the welfare needs of animals in varying housing
conditions and highlight areas in need of further attention and research.
Keywords: aardvarks, gorillas, drills, animal welfare, zoo, endocrinology
INTRODUCTION
Animal welfare science has advanced greatly in the last several decades.
This trend is also evident in the zoo and aquarium community, where
resources are increasingly being dedicated to better understanding how
captivity impacts animals and how best to assess and improve the welfare of
individual animals living in the care of humans. That said, the strides taken to
improve animal care, or the basic provisioning for animals’ needs, far outpace
efforts going beyond that to ensure great welfare. Meeting basic needs is
critical; however, good care does not necessarily translate to good welfare
(Rushen & de Passille, 1992; Kagan & Veasey, 2010; Kagan et al., 2015).
There is a difference between what humans provide for animals in their care,
and what each animal chooses to do with those provisions and how he or she
experiences the world as a result. Welfare is therefore the animals’ perceptions
of their psychological and physical states at any point in time.
There is still a lack of understanding of the needs of numerous species
living in zoos (Fidgett et al., 2008), and more research is necessary to increase
knowledge of factors that impact animal wellbeing. This includes
consideration of their lives 24 hours a day, year-round (Horback et al., 2014).
The practice of housing animals in behind-the-scenes or holding areas during
non-open hours is prevalent (Ross et al., 2010), and can often result in animals
being in less enriched and stimulating spaces for much of the 24-hour day,
which may for some include their active periods (Hoy et al., 2010). Traditional
Roles of Time and Space in Zoo Animal Welfare 3
behind-the-scenes holding spaces differ greatly from habitats, both in

complexity and size. The impact of such spaces is often overlooked and most
scientific inquiries into zoo animal behavior remain focused on daytime
observations in primary habitats (Ross et al., 2010). Complete welfare
assessments need to take all aspects of the environment, including the impact
of alternate spaces and differences in time of day, into consideration.
Some institutions have taken the necessary steps to house animals in their
primary habitats for much of the day, but there still remains a gap in providing
them with stimulating experiences after hours (Hoy et al., 2010). For some
species which are more active when zoo staff are not present, this can
represent a challenge as fewer behavioral opportunities may be available to
them. However, captive environments, both social and physical, should be
sufficiently complex to provide for great welfare regardless of the time of day
(Horback et al., 2014). Habitat design, which incorporates features that allow
animals to make meaningful choices and to engage in species-typical
behaviors, is a key factor in providing great animal welfare (Kagan & Veasey,
2010). Additional challenges may be present if some species cannot be housed
in their primary habitat for periods of the year due to weather fluctuations to
which they cannot acclimate. Appropriate species selection for a region’s
climatic conditions can alleviate this problem to a certain extent, but
committing resources to alternate housing options that offer the same level of
stimulation is also important. However, in cases where this is not possible,
careful assessment of the impact alternate housing has on the animals must be
undertaken. Deficiencies then need to be understood and rectified to alleviate
negative welfare consequences. Animal-related issues can also change the way
animals need to be housed. The need to separate animals at times can create
situations where individuals lack access to primary spaces or need to be
rotated between spaces. Assessment of the impacts on individuals in such
instances must also occur to ensure none of the individuals are compromised.
Beyond the challenges of providing for great animal welfare, there are
also challenges in assessing welfare. One major hurdle is our lack of certainty
in which measures are most relevant (Broom, 1991) and if the measures we
identify truly reflect the welfare status of an individual (Mendl, 1991). Animal
welfare science in zoos has grown out of animal behavior science, which has
been a part of the zoo community’s initiatives for many years. Tools being
employed to study the welfare of zoo animals focus largely on behavior
assessments and have grown to also employ endocrinology, primarily to
evaluate stress levels (Whitham & Wielebnowski, 2013). New efforts are
being deployed to examine additional hormonal measures, some focused on
indicators of positive welfare, rather than simply focusing on the absence or

reduction of stress (Boissy et al., 2007). A major benefit of using hormones
from excreta is that most can be obtained fairly non-invasively, as opposed to
blood sampling. Hormones can be measured in many bodily secretions and
from somewhat easily obtained materials such as hair and feathers as well
(Russell et al., 2012; Borlotti et al., 2008). There are still challenges associated
with this particular set of indicators, including cost and ability to ensure
hormonal responses truly reflect welfare impacts (Rushen & de Passille,
1992).
A major challenge has been to find means to evaluate the emotional states
of animals, which primarily relies on inferences from behavior, some use of
psychological testing including cognitive bias and preference tests (Mendl et
al., 2009; Bethell, 2015; Duncan, 2005; Kirkden & Pajor, 2006; Shapiro &
Lambeth, 2010), as well as the use of questionnaires developed to gain
knowledge indirectly about animal personality and wellbeing as rated by staff
persons knowledgeable of individual animals (Whitham & Wielebnowski,
2009; Tetley & O’Hara, 2012).
Other issues include reliably finding ways to assess the welfare of animals
when zoo staff are not present and in such a way as to not disturb and inflict
potential stress on the animals through the act of collecting information on
indicators of welfare. The use of video equipment is a common practice but
comes with its own set of challenges. Although technology has advanced,
leading to clearer images and greater ease of use, the cost can still be
prohibitive for some and the labor required to properly code and analyze data
may also be a hindrance in some cases. However, this is a more reliable way to
observe animals in situations where direct, live observations are not possible.
It is clear that multiple measures are necessary to obtain as complete of a
picture of the animal’s experience as possible (Hill & Broom, 2009). As
welfare encompasses an individual animal’s physical, mental and emotional
experience, indicators that reflect all of the dimensions are important.
Different situations will often dictate which means are most useful, as well as
those that are most feasible. Ongoing efforts to identify and validate animal
welfare measures are needed to ensure that zoos are ensuring great welfare for
animals.
The Detroit Zoological Society’s Center for Zoo Animal Welfare was
created in order to advance animal welfare science and policy, and one of the
major initiatives of the center is to conduct applied animal welfare research.
Two recent studies have been undertaken to better understand the impact that
night-time housing has on the welfare of animals residing at the Detroit Zoo.
These projects, including their methodological challenges and ensuing results,

are described along with recommendations for future research.
CASE STUDY 1-GORILLA/DRILL NIGHT HOUSING

Introduction
The Detroit Zoo is home to three male silverback Western lowland

gorillas (Gorilla gorilla gorilla) who share their habitat with two male drills
(Mandrillus leucophaeus). One of the drills was diagnosed with diabetes in
2014, leading to a number of husbandry changes to enable monitoring and
management of his condition. Prior to this, all five individuals shared space for
the majority of the 24-hour day, other than during habitat cleaning and for
purposes of positive reinforcement training. The gorillas and drills could be
housed together in an indoor habitat, an outdoor yard, or with access to both.
The specific area varied seasonally and was determined based on weather
conditions and temperature. After the diabetes diagnosis, night-time housing
was altered and resulted in the drills and gorillas alternating who would have
access to the indoor habitat and/or outdoor yard, with the other species staying
overnight in individual behind-the-scenes holding areas. These spaces varied
in both size and complexity, as well as in access to social partners. Both
factors have been found to impact welfare in non-human primates (Aureli &
de Waal, 1997). Overnight housing in behind-the-scenes holding areas is a
traditional practice for many species of zoo animals, but little research has
explored the impact that this may have on individual animals. Being restricted
in smaller spaces has been associated with indicators of negative welfare (see
Morgan & Tromborg, 2008); it is important to understand the effect that
spatial restrictions have on animal wellbeing (Herrelko et al., 2015).
A study was developed to examine the impact that the various night-time
housing conditions have on the individuals, prompted by questions from the
animal care staff working with them. The zoo keepers reported that the gorillas
behaved differently on mornings after they had spent the night singly-housed
in holding. Specifically, we examined the impact of night-time housing on the
welfare of the individuals as evidenced by their fecal glucocorticoid metabolite
(FGM) concentrations and their demeanor each morning as assessed by
experienced animal keepers. Animal care professionals are well suited to make
qualitative assessments of the animals in their care (Wemelsfelder et al.,
2007), and such assessments have been suggested as potential tools for animal
welfare evaluations (Wemelsfelder et al., 2001). Caretaker ratings of

behavioral profiles have indeed been deemed reliable (for review, see Tetley &
O’Hara, 2012), and thus in combination with the keeper reports of behavioral
differences based on night-time housing, we selected behavior questionnaires
as proxies for behavioral indicators of welfare.
Methods
Subjects and Housing

The subjects of this investigation were three male gorillas (Gorilla gorilla
gorilla) and two male drills (Mandrillus leucophaeus) residing in the Great
Apes of Harambee habitat at the Detroit Zoo in Royal Oak, MI. The gorillas
are half-brothers who were captive born and parent-reared, and who moved to
the Detroit Zoo in 2003 as subadults. Their ages at the time of data collection
were: Chipua (“Chip”), 19 years; Kongo-Mbeli (“Kongo”), 17 years; and
Pendeka (“Pende”), 18 years. The drills were also half-brothers born in
captivity who have been at the Detroit Zoo since 2008. At the time of data
collection, Aiku was 12 years old and Enwe was 14 years old.
The gorillas and drills were housed together during the day but separated
at night. Daytime housing conditions for the mixed-species group consisted of
a 2274 m2 outdoor yard, an indoor habitat, or access between the two. The
indoor habitat is 6.7 m in height with a domed ceiling and a trapezoidal floor
measuring about 200 m2. Generally, the group was given access to both the
yard and dayroom or confined to the yard at temperatures above 7°C, with
dayroom access more common on days with precipitation. At night, the two
species were separated and housed either in the indoor habitat or a behind-the-
scenes holding area. In the holding area, the gorillas were separated from one
another in adjacent stalls measuring 3.2 m (l) x 2.1 m (w) x 3.4 m (h). In this
space, the gorillas had visual and some tactile access to one another through
mesh doors separating the stalls. The drill holding area was located on the
other side of the building from gorillas, and the drills were also housed there in
separate stalls with contact through mesh doors separating stalls. Each drill
had access to a trapezoidal area of 4.1 m2 with a height of 3.1 m. Thus, each
single-species pair/trio was housed socially when spending the night in the
indoor habitat, while each individual was housed solitarily when that species
spent the night in the holding area.
For the purpose of this study, the gorillas and drills were rotated every
third night between the indoor habitat or the holding area. Thus, the gorillas
would spend two nights in the indoor habitat while the drills stayed in holding,
and then the gorillas would spend the next two nights in holding while the
drills stayed in the indoor habitat. On occasion, staff were unable to shift
animals to the planned night location. This generally happened when Aiku
would decline to leave the indoor habitat and enter the holding area at night.
When this happened, the schedule would reset on the next night. The total
number of nights spent in each location are summarized with daytime
locations in Table 1. Regardless of night location, each gorilla and drill was
moved into the holding space first thing in the morning for about two hours in
order for the keepers to service the habitats. During this period, the animals
were fed a portion of their daily diet and participated in positive reinforcement
training sessions with keepers.
Table 1. Sample totals for the study of welfare impacts of night housing
locations for gorillas and drills. Keeper assessments were completed in the
morning. Assessment totals refer to the location where the subjects spent
the previous night for night location in combination with their daytime
location when assessments were completed. To account for the lag time in
fecal hormone excretion, fecal sample totals refer to the location where
the subjects spent the previous night and their location the day previous
to fecal collection
Night Day Location Keeper Keeper Fecal Fecal

Location Assessments: Assessments: Samples: Samples:
Gorillas Drills Gorillas Drills
#Chip.Kongo. #Aiku.Enwe #Chip.Kongo. #Aiku.Enwe
Pende Pende
Indoor outdoor yard 7.7.7 3.5 13.17.14 8.9
Habitat indoor/outdoor 6.6.6 12.11 12.13.8 11.8
access
indoor habitat 5.5.5 4.2 5.5.4 2.3
Holding outdoor yard 6.6.6 7.6 16.16.16 17.17
Area indoor/outdoor 12.12.12 6.7 14.14.14 13.14
access
indoor habitat 2.2.2 5.6 8.8.7 4.4
Caretaker Assessments of Behavior

Caretakers completed assessments of each individual’s behavior in the
mid-morning after they were moved into their primary habitat for the day.
Ratings compared here were completed from March 8 to May 10, 2016, with a
two-week break in data collection during April. Raters were instructed to

observe the group for 15 minutes immediately after moving the animals to
their daytime habitat, and to base their assessments on the behavior observed
in the habitat during that time, as well as their behavior during and cooperation
with husbandry and training procedures while in holding during the morning.
Ratings were completed daily by one to three caretakers (either keepers or an
area supervisor). Raters were instructed not to discuss their ratings with one
another until all assessments had been completed for the day.
The behavior assessment tool (Table 2) was developed through a
combination of consulting primate care staff at the Detroit Zoo, modifying the
Gorilla Behavior Index (Gold & Maple, 1994), and modifying the gorilla
assessment developed for Brookfield Zoo’s WelfareTrak (Whitham &
Wielebnowski, 2009). The tool is based on a modified Likert scale, where the
rater codes on a 1 to 5 scale the level at which each animal’s behavior was
described by the questionnaire statement. Raters were permitted to score
values between levels (e.g., scores of 1.5 or 2.5) and to score not applicable if
they were unsure which rating to choose. Additionally, raters were instructed
to inspect each animal for new wounds acquired overnight and to score those
using the rating scale from Leeds et al. (2015). Only one wound was recorded
during the study period, and this measure is not included in further analyses.
Table 2. Final behavior assessment tool for gorillas and drills
Behavior Item
Activity
1. Very low: activity is very reduced from normal levels; not exploring food and/or
enrichment upon entering the habitat; very little movement
2. Low: activity is somewhat reduced from normal; upon entering the habitat, may
quickly grab a few food/enrichment items and sit or lie down to examine them
3. Moderate: sitting or lying down healthy amounts; interacting with conspecifics, food
and/or enrichment items and moving at a normal rate; upon entering habitat, explores
most of the area, checking out different food/enrichment items available
4. High: moving at an elevated pace; frequently changing locations and continuously
foraging upon entering the habitat
5. Very high: moving very rapidly from one location to the next in an unfocused
manner; restless; quickly losing interest in enrichment or conspecific/caretaker
interactions; spending little to no time lying down or sitting
Aggression towards conspecifics
1. Very low: showing almost no aggressive display behavior
2. Low: performing some displays such as chest-beating, head bobbing, or smacking
objects; these are occurring infrequently and are usually (but not always) undirected
3. Moderate: performing regular displays directed towards conspecifics
4. High: performing high-intensity displays directed towards conspecifics; attempting

physical aggression occasionally
5. Very high: very frequently performing directed displays; charging at or attempting to
grab/contact other individuals through mesh
Aggression towards humans
1. Very low: showing almost no aggressive behavior in the form of displays, grabbing,
or attempted contact aggression
2. Low: performing a couple of displays such as chest-beating, head bobbing, or
smacking objects in the presence of humans
3. Moderate: performing several displays towards humans; is still generally cooperative
and not grabby
4. High: displaying frequently at humans but not frequently attempting to grab or cause
harm; producing warning vocalizations at humans
5. Very high: frequently displaying at humans and vocalizing negatively; repeatedly
attempting to grab humans or nearby objects; attempting to cause physical harm to
humans
Anxiety
1. Very low: moving with confidence and relaxed posture; self-scratching or other
idiosyncratic movements are absent
2. Low: rating is between a 1 and a 3
3. Moderate: exhibits slightly elevated levels of self-scratching or other self-directed
behaviors; movements may be hesitant or guarded; or shows some evidence of minor
muscle tension, sweating, or fatigue
4. High: rating is between a 3 and a 5
5. Very high: reacting fearfully to almost all environmental stimuli; is trembling,
twitching, or shaking frequently; exhibits high levels of self-scratching or other self-
directed behaviors; appears very tense, distracted, or fatigued
Appetite
1. Very low: having no appetite; refusing to eat even favored foods, hand-fed treats or
food-related enrichment
2. Low: partially consuming diet but not enthusiastically; eating mainly preferred items
3. Moderate: readily consuming diet and showing preference for favored items; taking
hand-fed treats and food-related enrichment as usual
4. High: consuming all preferred items quickly and consuming all (or nearly all) the diet
in a short period of time
5. Very high: eating all diet items quickly and soliciting for additional food
Cooperation with husbandry and training
1. Very low: refusing to shift even after multiple requests; refusing to participate in
husbandry or training activities; or actively disrupting activities by grabbing at keepers,
throwing objects, or displaying
2. Low: shifting only after multiple requests; participating in husbandry and training but
frequently breaking attention from the task at hand or has to be asked multiple times to
comply with requests; may be refusing to perform some less favored tasks
3. Moderate: participating in husbandry and training procedures; readily shifting
between enclosures
Table 2. (Continued)
5. Very high: readily shifting and cooperating in procedures; but directing almost all
attention towards caretakers and as a result showing little interest in food, enrichment,
or conspecifics; repeatedly soliciting caretakers or attempting affiliative contact
Curiosity
1. Very low: showing very little interest in people, conspecifics, or the surrounding
environment; even ignoring novel or usually favored enrichment items; paying little
attention to surroundings; does not show interest in what keepers are doing or look
around to localize the source of noise/movement around him
2. Low: rating is between a 1 and a 3
3. Moderate: showing a moderate level of interest in his surroundings, such as watching
what keepers are doing, peering through mesh, trying to localize or observe activity of
people and/or conspecifics; if novel stimuli are present, is readily exploring new
situations, environments, objects, or people with reasonable caution
5. Very high: interacting with people, objects, or situations so intensely that
maintenance behaviors such as feeding are reduced; spending an excessive amount of
time exploring the environment; is frequently/easily distracted from normal
training/husbandry tasks
Dominance
1. Very low: giving in readily to others; reacting with fear and anxiety towards
conspecifics; consistently losing in competition for resources
2. Low: avoiding agonistic conflict with conspecifics; obtaining fewer resources relative
to conspecifics but is not always out-competed
3. Moderate: exerting dominance for highly-valued resources or in certain situations
only; is sometimes dominant and sometimes subordinate depending on the nature of the
interaction or the social partner
4. High: consistently asserting himself in competition for resources or attention;
frequently displacing other individuals from preferred locations; performing regular
dominance displays
5. Very high: hoarding resources; behaving aggressively towards all conspecifics and
antagonizing others for seemingly no reason; frequently performing dominance displays
Irritability
1. Very low: is not reacting negatively at all to people or conspecifics, even in conflict
situations; posture is extremely relaxed and loose
2. Low: does not become frustrated by waiting while others are fed or trained; may
show minor, transient tightening of posture or expression when provoked
3. Moderate: exhibits signs of frustration including grunting, pushing items away, or
other negative posturing (crossing arms, stiff-legged stance or walk) or expressions
(tight-lipped face, head-shaking, or piloerection)
4. High: is short-tempered or avoidant; showing prolonged negative responses in
postures or expressions
5. Very high: easily angered; reacting negatively with little or no provocation; showing
negative expressions almost constantly; producing negative vocalizations frequently;
and showing almost constant negative posturing
Regularity
1. Very low: producing little to no stool; may be observed straining to defecate;
constipated
2. Low: defecating less than usual; stools are drier, smaller, or darker in color than
normal
3. Moderate: defecating reliably at usual times; producing round, compact stools of a
normal size
4. High: stool is runny and less compact than normal, may be defecating at a slightly
elevated rate
5. Very high: diarrhea; frequently defecating with loose, watery stool
Undesirable behaviors
1. Very low: showing no evidence (either observed directly or indirectly, such as
showing new areas of missing fur) of stereotypic or undesirable behaviors, including
coprophagy, regurgitation and reingestion, hair-plucking, or wound-picking
2. Low: showing some evidence of undesirable behavior; performs one or more of the
above behaviors but only once or twice
3. Moderate: performing undesirable behaviors repeatedly, i.e., more than two bouts are
observed but are short-lasting and not intense
4. High: repeatedly observed performing undesirable behavior; performing a single
behavior repeatedly in rapid succession
5. Very high: extremely high rate of undesirable behavior; also showing some evidence
of harm caused by the behavior, such as irritation at wound or plucking sites
Overall assessment for today
Overall, how would you describe this individual’s wellbeing today?
1. Very low
2. Low
3. Moderate
4. High
5. Very high
Before the onset of data collection, the draft behavior tool was validated
by assessing inter-rater reliability. Eight primate keepers and an area
supervisor completed a draft of the assessment for each gorilla and drill. For
validation, raters were asked to consider how well each rating described the
typical behavior of the gorilla or drill. Inter-rater reliability was then assessed
using intra-class correlation coefficients. Validation results for the items
retained in the final version of the assessment (Table 2) are listed in Table 3.
Items discarded for having poor inter-rater reliability included: confidence,
equanimity, friendliness, happiness, mental agility, physical discomfort, and
understanding.
Table 3. Inter-rater reliability measures from validation of gorilla-drill

behavior tool
Item ICC ICC Cronbach’s

(3,k) (3,1) alpha
Activity 0.672 0.204 0.672
Aggression towards conspecifics 0.841 0.398 0.841
Aggression towards humans 0.943 0.673 0.943
Anxiety 0.724 0.247 0.724
Appetite 0.867 0.449 0.867
Cooperation with husbandry and training 0.867 0.483 0.867
Curiosity 0.845 0.405 0.845
Dominance 0.943 0.675 0.943
Irritability 0.833 0.384 0.833
Regularity 0.964 0.769 0.964
Undesirable behaviors 0.291 0.049 0.291
Overall assessment of wellbeing 0.567 0.141 0.567
Hormone Sample Collection and Analysis

Animal care staff collected daily morning fecal samples from each gorilla
and drill from March 8 to June 13, 2016. Fecals were generally collected while
the gorillas were separated for their morning feed, but times of sample
collection ranged from 0730 and 1500 h. One gorilla and one drill were
routinely fed glitter (Fuller et al., 2011) to facilitate identification of samples
collected from the indoor habitat. Fecals were labeled and stored at -20°C until
analysis. Samples were analyzed for fecal glucocorticoid metabolites in the
endocrinology laboratory at the Detroit Zoo.
Prior to extraction, fecal samples were lyophilized for approximately 32
hours. Dry samples were pulverized and sifted into a fine powder. For
hormone extraction, 0.2 +/- 0.01 g of fecal powder was combined with 2 ml of
90% ethanol, briefly vortexed, shaken for 30 min on a multi-tube mixer, and
centrifuged for 20 min at 2500 x g at 4°C (Peel et al., 2005). The supernatant
was poured off into a clean glass tube and dried under nitrogen gas at 35C.
Dried samples were stored frozen and reconstituted in assay buffer
immediately prior to analysis.
Fecal glucocorticoid metabolite (FGM) concentrations were measured
using a multi-species enzyme immunoassay for cortisol (Catalog #ISWE002;
Arbor Assays, Ann Arbor, MI). Cross-reactivities for this assay measured by
Arbor Assays are: 100% for cortisol, 42% for dehydrocortisol, 26% for
cortisone, 4% for dexamethasone, 3% for prednisone, 0.3% for
cortiscosterone, 0.2% for desoxycorticosterone, and < 0.16% for

tetrahydrocorticosterone.
The assay was chemically validated for gorillas and drills by analyzing
parallelism and recovery results. Serial dilutions (n = 7) of pooled gorilla
extracts showed parallel displacement to the standard curve (ANCOVA, F1,12
= 0.3, p = 0.4), as did serial dilutions of (n = 7) pooled drill fecal extracts
(ANCOVA, F1,12 = 0.1, p = 0.8). Recoveries of pooled gorilla samples spiked
with 800 pg/ml and 100 pg/ml of standard were 118% and 103%, respectively.
Drill recoveries were 121% with 800 pg/ml standard and 115% with 100 pg/ml
of standard. Both gorilla and drill samples were analyzed at a 1:8 dilution,
which corresponded to 58% binding for gorillas and 52% for drills. Each
sample was run in duplicate on a randomly assigned plate with three internal
controls at 75, 55, and 21% binding. The average inter-assay coefficient of
variation was 4.4% and the average intra-assay coefficient of variation was
2.6%. Final hormone concentrations were adjusted for dry weight and
expressed in ng/g dry feces.
Finally, the assay was biologically validated for stress opportunistically by
collecting fecal samples from each gorilla around (five days before and after) a
regularly scheduled veterinary exam in December, 2015. All three gorillas
were immobilized on the same day in the following order: Chip, Pende,
Kongo. Based on these results, dates for FGM concentrations are adjusted
backwards by 24 hours to match samples to housing conditions to account for
lag time to hormone excretion.
Data Analysis
Gorilla and drill behavior ratings were averaged among raters for each
day. Daily averages were non-normally distributed and were compared using
nonparametric Mann-Whitney tests. Correlations between daily mean ratings
and FGM concentrations were examined within species using non-parametric
Spearman rank correlations. Log-transformed FGM data was normally
distributed and was compared between housing conditions using generalized
linear mixed models with normal distributions and identity link functions.
Separate models were analyzed for gorillas and drills as groups, each including
subject ID as a random factor and three fixed factors: location the day before
the fecal was collected (indoor habitat, outdoor yard, or accessed between the
two), location the night before the fecal was collected (indoor habitat or
holding area), and an interaction term for day x night location. The number of
nights in a given night location (which ranged from 1 to 4) was also included
as a fixed factor but was non-significant and removed from final models.
Sample collection time was also non-significant both as a main effect and as
an interaction with both day and night location and was removed from final
models. Additional models with the same structure were created for each
individual subject without the random effect term. Degrees of freedom for all
models were calculated using a Satterthwaite approximation. Pairwise
comparisons were adjusted for multiple comparisons using the least significant
difference. Although we recognize the perils of using inferential statistics to
analyze data from individuals, we felt that the statistics would be informative
as to the magnitude of the effects of housing condition on individual welfare.
However, we do not recommend that these findings be extrapolated to gorillas
or drills in other housing situations.
Results
Behavior Assessment Data

Comparing mean daily assessment ratings completed mornings after the
drills spent the night in holding versus nights in the indoor habitat, there were
significant differences for activity, cooperation with husbandry and training,
and regularity. The drills were rated as more active after nights in the indoor
habitat (U = 474.0, p = 0.002) but were rated as more cooperative with
husbandry procedures after nights in the holding area (U = 376.5, p < 0.001).
Ratings for regularity were higher, indicating less firm stool, after nights in the
holding area compared to the indoor habitat (U = 434.5, p = 0.005). There was
also a trend of higher ratings for aggression towards humans after nights in the
indoor habitat (U = 528.5 p = 0.068).
For Aiku alone, the above trends for cooperation with husbandry and
training and regularity were consistent with group trends, and both were rated
higher after nights in the indoor habitat compared to the holding area
(cooperation, U = 85.0, p = 0.008; regularity, U = 93.5, p = 0.017). Aiku also
showed a trend towards higher ratings for appetite after nights in the indoor
habitat compared to holding (U = 112.0, p = 0.075).
Individually, Enwe was also rated as more cooperative with husbandry
after nights in holding compared to nights in the dayroom (U = 104.5, p =
0.042). He also showed a trend of higher ratings for activity (U = 112.0, p =
0.075) and aggression towards humans (U = 110.0, p = 0.066) after nights in
the dayroom than after nights in the holding area.
For the gorillas as a group, significant differences in caretaker ratings
were found comparing nights in holding to nights in the indoor habitat for
activity, regularity, and overall welfare. The gorillas were rated as more active
(U = 897.0, p < 0.001) and as having better overall welfare (U = 924.0, p <
0.001) after nights in the dayroom. The gorillas also had higher ratings for
regularity (looser stool consistency) after nights in holding compared to the
indoor habitat (U = 1380.0, p = 0.019). There was also a trend for higher
scores for anxiety after nights in holding (U = 379.5, p = 0.054).
Individually, each gorilla was rated as more active following nights in the
dayroom compared to holding (Chip, U = 107.5, p = 0.033; Kongo, U = 95.5,
p = 0.012; Pende, U = 96.0, p = 0.013). Kongo and Pende were both rated as
having higher overall welfare after nights in the dayroom (Kongo, U = 91.0,
p = 0.009; Pende, U = 100.5, p = 0.019), and this trend neared significance for
Chip (U = 116.0, p = 0.063). Kongo also showed a trend towards significantly
higher anxiety ratings after nights in holding compared to nights in the
dayroom (U = 37.0, p = 0.088).
Biological Validation of FGM Assay for Gorillas

FGM concentrations in fecals collected the day after veterinary exams
were elevated more than two standard deviations above baseline for both
Kongo (baseline mean + SD = 339.0 + 132.7 ng/g dry feces) and Pende
(baseline mean + SD = 380.1 + 105.4 ng/g dry feces) (Figure 1). FGM
concentrations for Chip, who was anesthetized first, did not show a similar
trend. FGM concentrations increased by 243.1% for Kongo compared to
baseline after the exam, while concentrations for Pende increased by 829.6%.
Concentrations returned to baseline levels in samples collected two days after
the exam for both gorillas.
Analysis of FGM by Housing Condition

For the drills together, FGM concentrations did not vary significantly
based on night location (F1,104 = 0.49, p = 0.48) but trended toward higher
concentrations in the yard compared to the indoor habitat (F2,104 = 2.50,
p = 0.09). There was no significant interaction between night and day locations
(F2,104 = 0.24, p = 0.79). There were no significant differences in FGM
concentrations in Aiku alone based on day (F2, 49 = 0.1, p = 0.89), night
(F1,49 = 0.57, p = 0.45), or particular combinations of the two (F2,49 = 1.22,
p = 0.30). Enwe showed a significant effect of day location (F2,49 = 3.23,
p = 0.048), with lower FGM concentrations when accessed between the indoor
habitat and yard during the day compared to the yard alone (t49 = -2.47,
p = 0.02). Enwe showed no significant effect of night location (F1,49 = 0.12,
p = 0.73) or interaction between night and day locations on FGM values

(F2,49 = 0.125, p = 0.88).
1200
a
1000
800
FGM (ng/g dry feces)
600
400
200
0
-5 -4 -3 -2 -1 0 1 2 3 4 5
Days from Vet Exam
3500 b
3000
2500
2000
1500
1000
500
0
-5 -4 -3 -2 -1 0 1 2 3 4 5
Days from Vet Exam
Figure 1. FGM concentrations measured in response to a regularly scheduled

veterinary exam for two male western lowland gorillas, Kongo (a) and Pende (b). The
solid horizontal lines indicate mean baseline concentrations, and the dashed horizontal
lines indicated the baseline mean + two standard deviations.
For the gorillas as a group, FGM values varied significantly based on day
location (F2,198 = 9.08, p < 0.001) and neared significance based on night
location (F1,198 = 3.84, p = 0.052); however, the effect of night location
depended on day location as shown by the significant interaction between the
two (F2,198 = 4.82, p = 0.009). Higher FGM concentrations for nights in
holding compared to the indoor habitat were most evident following days
when the gorillas had access between their two habitats (t198 = 3.64, p <
0.001). FGM concentrations were also generally higher on days in the yard
compared to the indoor habitat (t198 = 2.84, p = 0.005) and on days in the yard
compared to days when the gorillas had access between the two habitats (t198 =
3.97, p < 0.001). However, values for the yard may have been inflated by an
agonistic interaction that occurred there during the study in which Kongo
received a small wound. FGM levels for Kongo and Pende were both elevated
more than two standard deviations above their baselines on this day.
Figure 2. Fecal glucocorticoid metabolite concentrations (FGM; mean + SE) for Kongo
on nights in the holding area compared to nights in the indoor habitat depending on
daytime location. (*) indicates p < 0.05 for pairwise comparisons in a generalized
linear mixed model.
For Chip alone, there were no significant impacts of night (F1,62 = 1.40,
p = 0.25) or day location (F2,62 = 0.51, p = 0.60), or their interaction (F2,62 =
0.64, p = 0.53), on FGM concentrations. Pende’s FGM levels were
significantly impacted by day location only (F2,57 = 7.80, p = 0.001), with
higher FGM concentrations in the yard compared to the indoor habitat (t57 =
3.66, p = 0.001) and in the yard compared to the access condition (t57 = 2.58, p
= 0.01). There were no effects for night alone (F1,57 = 0.41, p = 0.53) or the
combination of night and day (F2,57 = 2.18, p = 0.12).
Kongo (Figure 2) exhibited significant differences in FGM concentrations
based on day location (F2,67 = 6.89, p = 0.002), with lower FGM values in the
indoor habitat compared to the yard (t67 = -2.12, p = 0.04) and when accessed
between the two habitats in comparison to the days in the yard (t67 = -3.60,
p = 0.001). Night location alone did not have a statistically significant effect
but neared significance for higher concentrations in the holding area compared
to the indoor habitat (F1,67 = 2.72, p = 0.10). FGM concentrations varied most
between the night housing conditions after days when Kongo had access
between the two habitats (F2,67 = 2.98, p = 0.06), with values trending upward
on nights in the holding area compared to the indoor habitat (t67 = 3.18,
p = 0.002), as for the group as a whole.
Correlations between Behavior Ratings and FGM Concentrations

For drills, Spearman correlations indicated that mean daily caretaker
ratings for aggression towards conspecifics, anxiety, and irritability were
significantly correlated with daily FGM concentrations. Higher ratings for
conspecific aggression ( = -0.3, p = 0.02), anxiety ( = -0.5, p = 0.001), and
irritability
( = -0.4, p = 0.007) were associated with lower FGM concentrations. Also,
higher scores for curiosity ( = 0.3, p = 0.06) were weakly associated with
higher FGM concentrations.
For gorillas, there were significant correlations between caretaker ratings
and FGM concentrations for aggression towards conspecifics and irritability.
Higher ratings for conspecific aggression ( = -0.3, p = 0.006) and irritability
( = -0.5, p < 0.001) were associated with lower FGM concentrations. Higher
caretaker ratings of activity were weakly associated with lower FGM
concentrations ( = -0.2, p = 0.06), while ratings of overall welfare showed a
weak positive association with daily FGM concentrations ( = 0.2, p = 0.07).
Conclusion
As evaluated by keeper ratings of behavior and fecal glucocorticoid

metabolite levels, the drills and gorillas in this study showed some signs of
being affected by the type of housing they inhabited overnight, but effects of
daytime housing appeared to be more impactful for these diurnal species. The
indoor habitat allows for social housing of both species, has more space and is
more physically complex than the individual holding stalls. Both species were
rated as more active and having more formed feces after spending the night
housed socially in the indoor habitat. Chimpanzees were found to locomote
more and display more species-typical behaviors when given access to a larger
space (Jensvold et al., 2001), and the primate species in this study may have
been adjusting their activity levels to match the amount of space available to
them. Additionally, the drills were perceived to be less aggressive towards

humans and more cooperative after spending the night singly-housed in the
holding stalls. It is possible that the drills were more eager to return to the
indoor habitat after nights spent in holding, impacting their demeanor in this
way. Aiku, who suffers from diabetes, was rated as displaying more signs of
having an appetite after nights spent in the indoor habitat. It is possible that
this space encouraged more activity for longer periods of the 24-hour day,
resulting in increases in his appetite level. Kongo was perceived to be more
anxious after nights spent in the holding stalls. Separation from conspecifics
has been linked to increases in stereotypic behaviors in a number of species
(for review, see Mason & Rushen, 2006), and for this individual gorilla, being
separated from social partners may be perceived as a negative experience.
Both the gorillas and drills were rated as having looser stool after nights
spent in holding than nights in the indoor habitat, a trend which may be related
to gut-stress interactions. Rhesus macaques (Macaca mulatta) in laboratory
housing show high incidences of chronic idiopathic diarrhea and colitis. A
retrospective review of risk factors predicting these disorders in rhesus
macaques found that housing type significantly predicted diarrhea rates,
whereby animals in smaller shelters and temporary housing areas showed
higher rates of diarrhea (Prongay et al., 2013). In human and animal models,
stress is known to play a causative role in the development of irritable bowel
syndrome through pathways that alter visceral sensitivity in response to
activation of the HPA (hypothalamic-pituitary-adrenal) axis (Larauche et al.,
2011). Given that the gorillas (although not the drills) trended towards higher
FGM concentrations after nights spent in holding, it is possible that differences
in stool quality between the two night-housing conditions were indicative of
levels of HPA activation, and possibly stress, overnight. However, a more
thorough investigation of the relationship between stool quality and HPA
activity, including how stool quality impacts FGM measurements taken in
feces, would be necessary to establish any causal relationships.
The behavioral assessments completed by the animal care staff showed
less variability and fewer correlations with housing condition than hoped,
which may be a result of the tool not being sensitive enough to capture what
may be very subtle signs exhibited by the drills and gorillas, instances of only
having one individual filling out the survey, low overall behavioral variability
in these species, or a combination of these factors. Although caretaker
assessments have been shown to accurately represent behavior profiles
(Wemelsfelder et al., 2007), it is possible that assessments of behavior being
exhibited several hours after waking may not be an accurate reflection of the
impact of night-time housing for drills and gorillas.
Interestingly, one of the few measures that reliably differed between night
housing conditions for the gorillas was the most subjective term, for which
caretakers were asked to rate the overall wellbeing of each animal for the day.
Other studies have found that measures of subjective wellbeing can be
collapsed into a single rating item, which for chimpanzees (Pan troglodytes)
correlates well with personality factors and submissive behavior (King &
Landau, 2003), and for capuchins (Sapajus apella) correlates with rates of
stereotypic behavior, as well as ratings of neuroticism and sociability
(Robinson et al., 2016). Measures of subjective wellbeing are also correlated
with personality dimensions in orangutans (Pongo spp.) that could translate
into differences in welfare; for example, individuals rated as less neurotic
received higher scores on subjective wellbeing measures (Weiss et al., 2006).
Perhaps caretakers who knew the animals well picked up on subtle differences
in behavior or signs of stress that were not captured in other assessment items
but were reflected in their subjective overall wellbeing scores.
Analysis of fecal glucocorticoid metabolites was conducted by night
location, location in which the primates were housed the previous day to
account for the aggregate nature of FGMs, and for any interaction of both
factors. For the drills, neither showed differences in FGM concentrations
based on where they spent the night, but they did show slightly higher levels
when they had spent the day in the outdoor yard versus the indoor habitat. This
may be a result of having a more drastic change in space allowance between
these two conditions. Additionally, Enwe’s FGM concentrations were the
lowest when he had access to both the outdoor and indoor habitats during the
day, regardless of where he spent the night. This daytime combination offers
the most choices, and having choices has been linked to improved welfare in
several species (Owen et al., 2006; Ross, 2006). When the drills were rated as
being more anxious, irritable, and displaying more aggression towards their
conspecifics, they had lower FGM concentrations.
In the case of the gorillas, daytime location had a significant impact and
night location approached significance, but this effect was due to the
interaction between the two factors. Concentrations of FGM were higher on
days when the gorillas were outside, although an instance of aggression
resulting in a small wound to one of the gorillas may have impacted those
results. Levels were highest for the group when they spent the night in holding
following days when they had access to both the outdoor and indoor habitats.
This may be a reflection of the impact of the more pronounced difference
between night-time housing that offered the least amount of choice following
the daytime condition that offered the most.
When looking at each gorilla individually, Chip showed no differences in
his FGM concentrations between any of the conditions. Pende on the other
hand, had higher concentrations when he spent the day outside. Kongo’s
concentrations were lower on days when he was accessed to both the indoor
and outdoor habitats, which represents the option with the greatest amount of
choice. His FGM concentrations also differed based on night condition on
days with access, with higher levels after nights in holding and lower levels
after nights in the indoor habitat. This may again reflect how a more marked
difference between amounts of available choice impacts individual gorillas.
That each individual responded differently is not unexpected, as stress
response results from an individual’s perception of his/her situation (Carlstead,
1998).
Similar to the drills, the gorillas had lower concentrations of FGM when
they were rated as more irritable and as being more aggressive towards their
conspecifics. Activity levels were also associated with lower FGM
concentrations, although this was not a strong relationship. Finally, there was
also a positive association between overall welfare and FGM concentrations.
Although this may seem counterintuitive, cortisol concentrations may not
always be closely linked to the mental or emotional states of animals (Rushen
& de Passille, 1992) and increases in FGM concentrations may be a response
to situations that are not regarded as stressful (Broom & Johnson, 1993).
Overall, none of the individual drills or gorillas were rated to display
negative indicators of welfare, such as undesirable behaviors. These results
suggest that alternating nights between two different types of indoor
environments which varied in size, complexity and access to social partners
did not have profoundly negative impacts on their welfare. However, the
trends toward higher FGM concentrations, lower overall welfare ratings, and
looser stool after nights in holding for the gorillas may warrant further
investigation and could suggest that overnight access to the group habitat
could have positive benefits for the gorillas. However, differences in FGM
concentrations were most evident on the individual level for Kongo, again
highlighting the point that welfare impacts vary on an individual basis, and
what is best for one individual may not apply to the group as a whole.
Comparing these results to data obtained when the drills and gorillas have
overnight access to an outdoor space would provide more information on the
importance of naturalistic features. Direct behavioral observations of both day-
time and night-time behavior may reveal stronger correlations between FGM
concentrations and behavior, elucidating the interplay between these welfare

measures.
CASE STUDY 2-AARDVARKS

Introduction
Aardvarks (Orycteropus afer) are solitary, nocturnal mammals native to

sub-Saharan Africa (Taylor et al., 2003). They are insectivores, feeding solely
on ants and termites (Taylor et al., 2002). Their activity patterns have been
found to vary slightly based on time of year, with length of time spent active
decreasing in the winter months (Taylor et al., 2003). They are considered to
be elusive and secretive (Taylor & Skinner, 2000), and there are few published
accounts of aardvark behavior and use of space, and almost no available
quantitative sources of information on captive aardvarks. As a result, an
understanding of their needs and how best to provide for their welfare is
largely reliant on anecdotal information. As nocturnal animals, aardvarks are
most active at times when zoo staff are not present, which can also present a
challenge when providing them with behavioral opportunities that can occupy
their time (Hoy et al., 2010).
The four aardvarks at the Detroit Zoo alternate between multiple indoor
spaces and one outdoor habitat depending on weather conditions and
temperatures. The indoor spaces are adjacent to one another and have shared
chain-link barriers permitting contact between inhabitants (Figure 3). Rotation
between multiple habitats has been shown to stimulate species-specific
behaviors in a number of species (Lukas et al., 2003; Hosey, 2005), although
this has not yet been investigated in aardvarks. However, proximity to
conspecifics who could be viewed through mesh barriers has also been shown
to increase pacing in some species (Bashaw, 2000), a behavior that can be
indicative of compromised welfare. The male aardvark housed at the Zoo was
noted to pace at times, and proximity to the oldest female with whom he had
sired multiple offspring was thought to be a potential contributing factor by
animal care staff. The spaces also varied in their access to environmental
features, with one having approximately half of the surface area covered in a
layer of dirt and the other two containing small tubs filled with pine shavings.
All contained at least one physical feature used for resting, either a plastic
culvert or a wooden nest box. The lower habitat contained a culvert, the front
habitat contained a large nest box, and the back habitat had one of each (See
Table 4 for further details). We developed a study designed to examine if the

aardvarks’ behavior and use of space was affected by the space to which they
had access, as well as the identity of their neighbor. Comparisons of the same
animals in different environments is aimed at identification of environmental
variables that impact behavior (Bashaw et al., 2007) and which features
individuals are selecting (Herbert & Bard, 2000). We used a combination of
behavioral data and hormone measures to explore the relationships between
space and social proximity for these aardvarks.
Figure 3. An illustration of the setup on the indoor habitats and the rotation. (A)
illustrates the first rotation and (B) illustrates the second rotation. The dotted lines
between habitats show the barriers allowing limited contact with neighbors.
Methods
The Detroit Zoological Society houses four aardvarks (Orycteropus afer).
Two aardvarks are singly housed, a thirteen-year old male, Baji, and a five-
year old female, Roxaane, and two aardvarks are co-housed, a twelve-year old
female, Rachaael, and her two-year old daughter, Kaatie. The male and
twelve-year old female are the parents of both younger aardvarks. All
aardvarks are rotated through three off-exhibit indoor habitats and one outdoor
habitat (weather permitting during the day). The three indoor habitats vary in
size, substrate, features, and contact with neighbors allowing the aardvarks
opportunities to perform different behaviors and socially interact with different
partners. Observations were performed during winter and spring months when
there was limited access to the outdoor habitat.
Table 4. Description of the three indoor spaces
Housing condition Features

(indoor space)
Front Habitat 1. Cement habitat with nest box and two small boxes with pine
shavings
2. Approximate area 37m2
3. Has shared barriers allowing contact with both the other
indoor habitats
Back Habitat 4. Cement habitat with nest box, plastic culvert, and a box with
shavings
5. Approximate area 26m2
6. Has a shared barrier allowing contact with the front habitat
Lower Habitat 7. Half cement and half dirt habitat with a plastic culvert
8. Approximate 43m2
9. Has a shared barrier allowing contact with the front habitat
Observations were broken down into two sections. The first section
consisted of eight weeks during which the normal habitat rotation with their
normal neighbors was followed. Eight weeks into the observation period the
rotation was changed; while the aardvarks experienced the habitats in the same
pattern, their neighbor in the next habitat was different than in the previous
rotation. For example, when the singly housed male was in the front habitat,
for the first eight weeks he was used to seeing the singly housed female in the
back habitat and the co-housed females were in the lower habitat. For the
second observation period, the co-housed females were in the back habitat
instead and the singly housed female was in the lower habitat. All females
were observed for eight weeks after the change in rotation. The male was
observed for another ten weeks. Six weeks into the second rotation, the male
received Deslorelin implants in order to determine if this would impact pacing
that was possibly related to the proximity of females, and the following four
weeks were used to assess any impact of the implants on his behavior.
Behavioral data was collected through videos downloaded with RealShot
Manager Advanced software (Sony Corporation, Tokyo, Japan). Each video
was thirty minutes in length and between the hours of 22:00 - 6:00 (23:00 -
7:00 with the start of daylight savings). Videos for each individual were
downloaded seven days a week from January 18, 2016 to May 25, 2016. There
was a total of 62.5 hours of video for Baji, 57.5 hours of video for Roxaane,
and 58 hours of video for Rachaael and Kaatie. Observation times were
balanced for housing condition and rotation. In addition, to decrease chances
of inflating behaviors impacted by conspecifics, each individual’s observation
for a specific night was scheduled to take place at a different time. Due to
some human and technical errors, there were six days where two aardvarks
shared the same observation time. None of these pairs of videos belonged to
both the co-housed females.
Table 5. Ethogram of aardvark behavior
Behavior Description
Affiliative Any positive social interaction between the focal and another individual.
Interaction Can include resting in contact, allogrooming, social play, etc.
Any negative social interaction between the focal and another
Agonistic individual. Can include displacing, being displaced, biting, hitting with
Interaction front limbs or torso, being withdrawn from/withdrawing from an attempt
at an affiliative interaction, etc.
Focal is using anterior and posterior limbs to remove dirt from a certain
Dig
area.
Drink Focal is ingesting water.
Focal is intaking and consuming food items that are not enrichment
Eat
items.
Explore Individual is investigating an enrichment object through touching,
Enrichment smelling, tasting, and/or visual inspection.
Focal is investigating an object in their habitat (not enrichment) through
Explore
touching, smelling, and/or visual inspection. Focal can be stationary or
Object
in motion.
Focal’s snout or anterior/posterior limbs are in contact with its own
Grooming
body.
Focal is in motion, traveling from one point of the exhibit to another,
Locomote
head is up off the ground.
Not visible Focal or their behavior is out of sight.
Other Any behavior not defined elsewhere, please make a note of the behavior.
Focal is in motion, but traveling the same route repeatedly. Must have
Pace
completed the circuit three times before considered pacing.
Focal is in a state of inactivity with their torso against the ground, there
Rest will be little to no bodily movement, head will be lowered and eyes may
be closed.
Focal is inactive with their torso against the ground, but their head is up.
Stationary -
Focal may be orienting towards an object/event or just scanning the
Lay
environment.
Focal is inactive, but supporting their weight on all four feet with their
Stationary -
torso off the ground. Focal may be orienting towards an object/event or
Standing
just scanning the environment.
Videos were coded by four individuals. Inter-observer reliability (IOR >

0.90) was assessed through coding of three 10-minute video segments before
observations began. Videos were coded using instantaneous scan sampling
occurring at one minute intervals for behavior (Table 5), location, and
substrate/features. For the purpose of this chapter, only the following
behaviors were analyzed: locomotion, rest, exploration, and pace behaviors. In
addition, time individuals spent near a shared barrier that allowed contact was
also examined.
For the purpose of this analysis, ‘not visible’ scans of more than 3 minutes
were all considered ‘presumed resting’ and added with ‘rest’ behavior scans to
gain a ‘total rest’ variable. In addition, ‘explore enrichment’ scans were added
to ‘explore object’ scans to gain a ‘total explore’ variable.
Hormone Sample Collection and Analysis
Animal care staff collected daily evening fecal samples from each
aardvark from January 13 to May 26, 2016. Sample collection time ranged
from 1300 to 2230. The two aardvarks housed together were fed concentrated
food coloring (gel paste) to identify individual fecals (Fuller et al., 2011).
Fecals were labeled and stored at -20°C until analysis. Samples were analyzed
for fecal glucocorticoid metabolites in the endocrinology laboratory at the
Detroit Zoo.
Prior to extraction, fecal samples were lyophilized for approximately 24
hours. Dry samples were pulverized and sifted into a fine powder. For
hormone extraction, 0.2 +/- 0.01 g of fecal powder was combined with 2 ml of
90% ethanol, briefly vortexed, shaken for 30 min on a multi-tube mixer, and
centrifuged for 20 min. at 2500 x g at 4°C. The supernatant was poured off
into a clean glass tube and dried under nitrogen gas at 35 C. Dried samples
were stored frozen and reconstituted in assay buffer immediately prior to
analysis.
Fecal glucocorticoid metabolite (FGM) concentrations were measured
using a commercial enzyme immunoassay kit for corticosterone (Catalog
#K014-H1; Arbor Assays, Ann Arbor, MI). Assay cross-reactivities according
to the manufacturer are as follows: 100% for corticosterone, 12% for
desoxycorticosterone, 0.8% for tetrahydrocorticosterone, 0.6% for
aldostesrone, 0.4% for cortisol, 0.2% for progesterone, 0.1% for
dexamethasone, and < 0.1% for corticosterone-21-hemisuccinate, cortisone,
and estradiol.
The assay was chemically validated for aardvarks by analyzing parallelism

and recovery results. Serial dilutions (n = 8) of pooled aardvark extracts
showed parallel displacement to the standard curve (ANCOVA, F1,14 = 3.3, p =
0.09). Recoveries of pooled samples spiked with 2,500 pg/ml and 312.5 pg/ml
of standard were both 93%. Samples were analyzed at a 1:3 dilution, which
corresponded to 51% binding on the standard curve. Each sample was run in
duplicate on a randomly assigned plate. Inter-assay variation was assessed
using two internal controls at 42 and 54% binding, and the average coefficient
of variation was 4.9%. The average intra-assay coefficient of variation was
2.4%. Final hormone concentrations are adjusted for dry weight and expressed
in ng/g dry feces.
Finally, the assay was biologically validated for stress opportunistically by
analyzing fecal samples from Baji, Kaatie, and Roxaane collected around (four
to five days before and after) regularly scheduled veterinary exams in March
and April of 2016 during the study period. We did not have a sample from
Rachaael the day after her exam. Samples collected the day after exams were
removed prior to analyzing trends in FGM concentrations in relation to
housing condition and rotation data and were used only for validation
purposes. Based on these results, dates for FGM concentrations are adjusted
backwards by 24 hours to match samples to housing conditions to account for
lag time to hormone excretion.
Data Analysis
Total scans for each behavior were summed by observation and were
compared between housing condition and rotation using a generalized linear
mixed model with negative binomial distribution and a log link function. Fixed
factors included housing condition (front, back, or lower), rotation (first or
second), and an interaction term for housing condition x rotation. A variance
component covariance structure and model fit were selected on the basis of
AIC (Akaike information criterion). Additional models with the same structure
were created for each individual subject without the random effect term.
Hormone implant (before and after) was also used as a fixed factor in the
model for Baji only. Degrees of freedom for all models were calculated using
a Satterthwaite approximation. Pairwise comparisons were adjusted for
multiple comparisons using the least significant difference. We were unable to
fit a mixed model for the aardvark pacing data, so totals for pacing were
compared using non-parametric Wilcoxon signed rank tests and Mann-
Whitney tests.
The total number of aardvark fecal samples analyzed per condition are
listed in Table 6. Aardvark FGM data were positively skewed even after
transformation, so untransformed hormone concentrations were analyzed using
a generalized linear mixed model with a gamma distribution and a log link
function. Fixed factors included housing condition (front, back, or lower),
rotation (first or second), an interaction term for housing condition x rotation,
and sample collection time. A variance component covariance structure and
model fit were selected on the basis of AIC (Akaike information criterion).
The variable collection time was not significant either as a main effect or as an
interaction with housing condition or rotation and was removed from final
models. Additional models with the same structure were created for each
individual subject without the random effect term. Fecal samples were not
collected from Rachaael during the first rotation, so the model included
housing condition as the only fixed factor. Implant presence was also included
as a fixed factor for Baji only. Degrees of freedom for all models were
calculated using a Satterthwaite approximation, and pairwise comparisons
were adjusted for multiple comparisons using the least significant difference.
Finally, bivariate correlations between the total number of scans for each
behavior per observation were compared to daily FGM concentrations using
non-parametric Spearman correlations.
Table 6. Total fecal samples analyzed for fecal glucocorticoid metabolites

based on individual aardvark, housing condition, and rotation
Rotation Housing Condition Baji Kaatie Rachaael Roxaane

One lower 6 1 0 1
front 16 15 0 12
back 18 10 0 16
Two lower 2 0 0 3
front 17 17 16 16
back 16 15 8 18
Results
Behavioral Assessment
While only specific behaviors were statistically analyzed, an overall
activity budget for each individual in the three housing conditions has been
included to help frame the results of the analyses (Figure 4). In addition, for
each individual, descriptive statistics of location and substrate/feature use have

been included with the results to help create an inclusive view of the data.
Figure 4. Activity budget for each individual aardvark broken down by housing
condition: Rachaael (a), Roxaane (b), Kaatie (c), and Baji (d).
Group
Overall, the aardvarks spent more time locomoting (F2,466 = 13.101, p <
0.001) and exploring (F2,466 = 4.437, p = 0.012) and less time resting (F2,466 =
4.715, p = 0.009) in the front habitat than in the back or lower habitats. In
addition, as a group, the aardvarks spent significantly more time by shared
barriers in the two habitats without dirt than in the habitat with dirt (F2,466 =
25.080, p < 0.001) and paced significantly more in the habitats without dirt
compared the habitat with dirt (Table 7 shows all significant statistics for pace
behavior). There was not a significant difference in the amount of pacing
between the front habitat and the back habitat.
There was a significant main effect for rotation when examining
locomotion (F1,466 = 4.022, p = 0.045) with more locomotion seen during the
first rotation than the second rotation. There was not a significant main effect
of rotation seen in resting (F1, 466 = 0.104, p = 0.747), exploring (F1,466 =1.061,
p = 0.303), or pacing behaviors. For the aardvarks as a group, there was no
interaction of housing condition and rotation seen for rest (F2,466 = 1.261, p =
0.284), exploration (F2,466 = 2.082, p = 0.126), or locomotion (F2,466 = 1.707, p
= 0.183).
Table 7. Results of pairwise comparisons for aardvark behaviors based on rotation, housing condition, and rotation
x housing condition. Pace behaviors were compared using pairwise Wilcoxon signed rank tests. All other behaviors
were compared using a generalized linear mixed model adjusted for multiple comparisons using the least significant
difference. P-values are reported for significant results where p < 0.05, and results where p > 0.05 are marked NS
for non-significant. NS* indicates a trend of 0.05 < p < 0.10
1st Rotation 2nd Rotation

1st vs. 2nd Front vs. Front vs. Back vs. Front vs. Front vs. Back vs. Front vs. Back vs.
Behavior Front vs.
Rotation Back Stall Lower Stall Lower Stall Back Lower Lower Lower Lower
Back Stall
Stall Stall Stall Stall Stall
t10 = 3.16, t22 = 2.61, t14 = 2.95, t27 = 2.49,
Locomote NS* NS NS* NS NS NS
p = 0.01 p = 0.02 p = 0.01 p = 0.02
t318 =
t200 = -2.66, t466 = -2.14, t229 = -2.57,
Rest NS NS NS NS NS -2.37, NS
p = 0.008 p = 0.03 p = 0.01
p = 0.02
t28 = 2.26, t32 = 2.18, t21 = 2.43,
All Explore NS NS* NS NS NS NS NS
p = 0.03 p = 0.04 p = 0.02
Aardvarks
z=
z = -3.29, z = -2.17, z = -2.05, z = -2.90,
Pace NS NS NS NS* -2.15, NS
p = 0.001 p = 0.03 p = 0.04 p = 0.004
p = 0.03
t20 =
Time Near a t61 = 2.23, t8 = 3.73, t16 = 3.12, t20 = 3.00, t30 = 2.66, t14 = 3.21,
NS NS 2.95, NS
Barrier p = 0.03 p = 0.01 p = 0.01 p = 0.01 p = 0.01 p = 0.01
p = 0.01
t109 =
t109 = -2.59, t109 = 2.14,
Locomote NS* NS NS NS NS* NS NS -2.26,
p = 0.01 p = 0.03
p = 0.03
Rachaael
t109 =
t109 = 2.19,
Rest NS NS NS* NS NS* NS NS* NS 2.29,
p = 0.03
p = 0.02
1st vs. 2nd Front vs. Front vs. Back vs. Front vs. Front vs. Back vs. Front vs. Back vs.
Behavior Front vs.
Back Stall
t109 = t109 = t109 =
t109 = 2.60,
Explore NS NS NS NS -2.44, -2.15, NS NS -2.09,
p = 0.01
p = 0.02 p = 0.03 p = 0.04
z = -2.26,
Rachaael Pace NS NS* NS NS NS NS NS NS NS
p = 0.02
cont’
t109 =
t109 = t109 =
Time Near a t109 = 3.32, t109 = 2.21, t109 = 2.27, -2.01, t109 = 2.84,
NS NS 2.53, NS* -2.35,
Barrier p = 0.001 p = 0.03 p = 0.025 p= p = 0.005
p = 0.01 p = 0.02
0.047
t108 =
t108 = t108 = t108 =
t108 = 4.43, t108 = 5.45, t108 = 4.16, 3.37, t108 = 2.83,
Locomote NS* 3.70, NS 3.86, 3.40,
p < 0.001 p < 0.001 p < 0.001 p= p = 0.006
p < 0.001 p < 0.001 p = 0.001
0.001
t108 =
t108 = t108 =
t108 = -4.11, t108 = -4.59, -3.16, t108 = -2.62,
Rest NS NS -3.11, NS -3.38, NS*
p < 0.001 p < 0.001 p= p = 0.01
p = 0.002 p = 0.001
0.002
Roxaane t108 = t108 = t108 = t108 =
t108 = 2.28, t108 = 4.20, t108 = 3.46,
Explore NS 2.16, 2.60, NS NS 3.10, 2.99,
p = 0.025 p < 0.001 p = 0.001
p = 0.03 p = 0.01 p = 0.002 p = 0.003
z = -3.31, z = -2.23, z = -2.03, z = -2.68, z = -2.06,
Pace NS NS* NS NS NS
p =0.001 p = 0.03 p = 0.04 p = 0.007 p = 0.04
t108 =
t108 = t108 = t108 =
Time Near a t108 = 3.80, t108 = 5.07, t108 = 4.92, 2.80,
NS* NS 3.21, NS 3.60, 3.54,
Barrier p < 0.001 p < 0.001 p < 0.001 p=
p = 0.002 p < 0.001 p = 0.001
0.006
Table 7. (Continued)

1 vs. 2
st nd
Front vs. Front vs. Back vs. Front vs. Front vs. Back vs. Front vs. Back vs.
Behavior Front vs.
Back Stall
t109 = 3.13, t109 =2.29, t109 =2.60,
Locomote NS NS NS NS NS NS NS*
p = 0.002 p = 0.02 p = 0.01
t109 =
Rest -2.05, NS NS NS NS NS NS NS NS NS
p = 0.04
Explore NS NS NS NS NS NS NS NS NS NS
Kaatie
z= z=
z = -2.32, z = -2.44, z = -2.42,
Pace NS -2.53, NS -2.53, NS NS NS
p = 0.02 p = 0.015 p = 0.01
p = 0.01 p = 0.01
t109 = t109 =
Time Near a t109 = 3.00, t109 = 3.31, t109 = 2.27,
NS NS NS* 2.60, NS 2.04, NS
Barrier p = 0.003 p = 0.001 p = 0.025
p = 0.01 p = 0.04
t118 = 3.42, t118 = -2.28, t118 = 3.13,
Locomote NS NS NS NS NS* NS* NS
p = 0.001 p = 0.02 p = 0.002
t118 =
t118 = -2.49, t118 = -2.65,
Rest NS NS NS NS NS NS -2.46, NS
p = 0.01 p = 0.009
p = 0.015
Baji Explore NS NS NS NS NS NS NS NS NS NS
z = -2.44, z = -2.21,
Pace NS* NS NS NS NS NS NS NS
p = 0.015 p = 0.03
t118 =
Time Near a t118 = 2.90, t118 = 2.05,
NS NS NS NS NS NS 2.70, NS
Barrier p = 0.005 p = 0.04
p = 0.008
Roles of Time and Space in Animal Welfare 33
Finally, there was a significant interaction for housing condition and

rotation for time spent at shared barriers (F2,466 = 3.285, p = 0.038). On average
the group spent more time at shared barriers in the front habitat after the
rotation change and less time at shared barriers in the back habitat. There was
also a significant effect for the pace behavior of rotation on housing condition.
In the first rotation, as a group, the aardvarks paced more in the back habitat
than in the lower habitat and trended towards pacing more in the front habitat
than the lower habitat. No significant difference was found in pacing between
the front and back habitats. However, in the second rotation, there was an
increase in the amount of pacing in the front habitat making it significantly
different from the back and lower habitats. There was no significant difference
between the back and lower habitats. Table 7 presents all the statistically
significant post-hoc pairwise comparisons.
Because welfare is a concept that affects the individual, analyses were
completed looking at each individual separately as well.
Rachaael
Rachaael spent the most time in the middle two locations which
encompasses 50% of the space of the front habitat away from the barriers
(80.96%, Standard Error: +/- 4.06%). In the back habitat, her location use
varied with rotation; in the first rotation Rachaael spent 46.83% (+/- 9.12%) in
the third of the habitat that is near the barrier and 24.50% (+/- 8.15%) in the
farthest location (a third of the habitat) from the barrier. In the second rotation,
she spent 1.30% (+/- 0.81%) near the barrier and 59.81% (+/- 11.28%) in the
farthest location from the barrier. In the lower habitat, Rachaael’s preference
did not change with rotation, she spent the majority of her time (57.67% +/-
5.69%) in 1/6 of the habitat that is located near the wall by the back habitat.
This area contained both dirt and the plastic culvert.
Rachaael spent the majority of her time in all habitats in either the nest
box (front habitat: 67.98% +/- 6.33%; back habitat: 3.60% +/- 2.65%) or the
plastic culvert (back habitat: 51.23% +/- 7.54%; lower habitat: 38.42% +/-
7.29%) which were the main resting areas. When dirt was available she spent
46.25% +/- 5.73% of her time on dirt. She was rarely seen in the boxes with
pine shavings (front habitat: 4.38% +/- 2.78%; back habitat: 15.70% +/-
5.21%). The rest of the time was spent on cement (front habitat: 27.63% +/-
5.80%; back habitat: 24.21% +/- 5.62%; lower habitat: 15.33% +/- 2.57%).
Rachaael’s locomotion (F2,110 = 4.703, p = 0.011) and pacing behaviors
were affected by housing condition, and there was a trend for housing to affect
rest as well (F2,110 = 2.94, p = 0.057). Rachaael showed more locomotion in
both the front habitat and the lower habitat than in the back habitat. However,
Rachaael averaged about 68.9% of her activity budget resting in the back
habitat compared to the 45% and 63.8% of time resting in the lower and front
habitats respectively. Rachaael paced more in the back habitat than the front
habitat and showed a trend to pace more in the lower habitat than the front
habitat. There was no significant difference in pacing between the back and
lower habitats. Exploration showed no main effect for housing condition
(F2,110 = 1.212, p = 0.302).
Rotation had no significant effect on Rachaael’s locomote (F1,110 = 3.050,
p = 0.084), rest (F1,110 = 1.011, p = 0.32), explore (F1,110 = 0.867, p = 0.354),
and pace behaviors.
There was a significant interaction between housing condition and rotation
for locomotion (F2,110 = 3.725; p = 0.027) and exploration (F2, 110 = 13.013, p <
0.001; Figure 5a), but not for rest (F2,10 = 2.40, p = 0.096). A further look at
the interaction shows an increase in exploration in the front habitat as well as a
decrease in exploration for both the back and lower habitats with the switch
from rotation one to rotation two. A similar trend was seen for locomoting
behavior. There was no significant effect of rotation on housing condition as
related to pacing.
Finally, in relation to time spent at shared barriers, Rachaael showed both
main effects of housing condition (F2,110 = 4.278, p = 0.016) and rotation (F1,110
= 14.873, p < 0.001) as well as an interaction of housing condition and rotation
(F2,110 = 16.507, p < 0.001). Rachaael drastically decreased her time spent by
the shared barrier in the back habitat in rotation two compared to rotation one
(See Figure 6).
Figure 5. Interaction of housing condition and rotation on Rachaael's (a) and Roxaane's
(b) time spent exploring. Error bars represent SE and (*) indicates p < 0.05 for
pairwise comparisons in a generalized linear mixed model.
Figure 6. Interaction of housing condition and rotation on the time Rachaael spent at a
shared barrier. Error bars represent SE and (*) indicates p < 0.05 for pairwise
comparisons in a generalized linear mixed model.
Roxaane
In the front habitat, Roxaane spent a large portion of her time in the area
by the barrier to the lower habitat with her time being increased from 39.67%
(+/- 6.75%) in the first rotation to 56.67% (+/- 5.47%) in the second rotation.
With the rotation change, she decreased her use of the area closest to the back
habitat from 27.33% (+/- 7.00%) to 11.58% (+/- 5.48%). In the back habitat,
Roxaane, regardless of rotation, spent just under half her time in the farthest
location from the barrier (48.72% +/- 6.33%) and over a third of her time in
the area closest to the barrier (38.46% +/- 6.26%). In the lower habitat,
Roxaane spent the majority of her time in the third of the exhibit located near
the back habitat (91.63% +/- 4.88%).
Roxaane was seen the majority of the time in the plastic culvert when
available (back habitat: 54.87% +/- 6.95%; lower habitat: 64.41% +/- 7.75%).
Although, she decreased her use of the plastic culvert from 80.37% (+/-
9.20%) in the first rotation to 49.30% (+/- 11.49%) in the second for the lower
habitat and decreased from 67.00% (+/- 9.08%) to 42.10% (+/- 10.00%) with
the rotation change in the back habitat. In the lower habitat, she preferred the
dirt (28.56% +/- 7.07%) over cement (7.03% +/- 3.40%). When dirt was not
available, she was found on cement (front habitat: 90.68% +/- 3.86%; back
habitat: 41.02% +/- 6.62%) more often than on pine shavings (front habitat:
0.26% +/- 0.14%; back habitat: 1.37% +/- 0.45%) or in the nest box (front
habitat: 9.06% +/- 3.87%; back habitat: 2.74% +/- 1.11%).
There was a significant main effect of housing condition for Roxaane’s
locomote (F2,109 = 34.821, p < 0.001), rest (F2,109 = 25.968, p<0.001), explore
(F2,109 = 17.456, p < 0.001), and pace behaviors. Roxaane showed more
locomoting and exploring in the front habitat compared to the other two
habitats. In addition, Roxaane paced more in the front habitat than the lower
habitat and trended towards pacing more in the front habitat than the back
habitat. Roxaane also paced more in the back habitat compared to the lower
habitat. However, Roxaane showed the least amount of resting behavior in the
front habitat compared to the other two habitats.
Roxaane showed no significant main effect of rotation on locomotion
(F1,109 = 2.293, p = 0.133), rest (F1,109 = 0.214, p = 0.645), and exploration
(F1,109 = 0.005, p = 0.944) behaviors. However, there were significant
interactions between housing condition and rotation for locomotion (F2,109 =
3.432, p = 0.036) and exploration (F2,109 = 4.338, p = 0.015; See Figure 5b).
Both behaviors showed the similar pattern of decreasing in the lower habitat,
but increasing in the back habitat when the aardvarks were switched from
rotation one to rotation two. There was no significant interaction for resting
behavior (F2,109 = 0.729, p = 0.485).
Although there was no statistically significant difference in the amount of
time spent pacing between the first and second rotations, the allocation of
pacing behavior among habitats depended on rotation order. In the first
rotation, Roxaane did not show a significant difference in pacing in the back
habitat compared to the front or lower habitats, but she spent significantly
more time pacing in the front habitat than in the lower habitat. During the
second rotation, Roxaane continued to pace more in the front habitat compared
to the lower. She also increased the amount of time spent pacing in the back
habitat, which became statistically significant compared to time spent pacing
in the lower habitat as well. As during the first rotation, the amount of time
spent pacing did not differ between the front and back habitats during the
second rotation.
When examining time spent at shared barriers, there was a significant
effect of both housing condition (F2,109 = 25.314, p < 0.001) and rotation (F1,109
= 10.531, p = 0.002) as well as a significant interaction between housing
condition and rotation (F2,109 = 6.130, p = 0.003). At three of the four shared
barrier combinations, Roxaane spent less time near the barrier when that
barrier was shared with the male and more time when the barrier was shared
with the co-housed females.
Kaatie
Kaatie’s location use did not vary much with rotation. In the front habitat,
she preferentially spent her time in a quarter of the habitat away from both
barriers (54.74% +/- 5.20%). In the back habitat, she spent 65.61% (+/- 5.55%)
of her time in the farthest third of the exhibit from the barrier. Finally, in the
lower habitat, she spent the majority of her time (65.41% +/- 4.84%) in the
third of the exhibit located by the back habitat.
While Kaatie spent a large amount of time in the nest box (front habitat:
42.28% +/- 6.44%; back habitat: 9.47% +/- 4.17%) or plastic culvert (back
habitat: 40.26% +/- 6.82%; lower habitat: 27.83% +/- 6.36%), she spent more
time on the dirt (lower habitat: 47.67% +/- 4.64%) and cement (front habitat:
56.93% +/- 6.37%; back habitat: 46.14% +/- 6.23%; lower habitat: 24.5% +/-
2.77%) than Rachaael, with whom she is co-housed.
Kaatie showed an effect of housing condition for her pacing behavior, as
Kaatie paced more in the back habitat compared to the lower and front
habitats. There was no significant difference in pacing between the front and
lower habitats. There was a main effect of housing condition on locomotion
that was trending towards significance (F2,110 = 3.029, p = 0.052), as Kaatie
locomoted more in the front habitat compared to the other habitats. There were
no significant main effects of housing condition seen on rest (F2,110 = 0.755, p
= 0.472) or exploration (F2,110 = 1.664, p = 0.194) behaviors.
There was a significant main effect seen for rotation when analyzing
Kaatie’s rest (F1,110 = 4.552, p = 0.035), locomotion (F1,110 = 10.900, p = 0.001)
and pace behaviors. Not only was Kaatie resting on average 15% more during
the second rotation compared to the first rotation, but her time spent
locomoting dropped roughly 10.5% from rotation one to rotation two. In
addition, her pacing had encompassed 1.7% of her activity budget in rotation
one but dropped to 0.11% of her activity budget in rotation two. There was no
significant main effect of rotation seen for exploration (F1,110 = 0.009, p =
0.923).
There was a significant change in Kaatie’s pacing with the effect of
rotation on housing condition. In the first rotation, Kaatie showed a significant
difference in her pacing in the back habitat compared to the front and lower
habitats. There was not a significant difference in her pacing when comparing
the front and lower habitats. In the second rotation, there was no significant
difference in her pacing between the habitats.
There were no significant interactions between housing condition and
rotation for locomotion (F2,110 = 2.446, p = 0.091), exploration (F2,110 = 0.177,
p = 0.838), or rest (F2,110 = 0.221, p = 0.802).
When examining time by shared barriers, there was no significant effect

for rotation (F1,110 = 0.217, p = 0.642) nor a significant interaction between
housing condition and rotation (F2,110 = 0.587, p = 0.558). There was a
significant effect of housing condition (F2,110 = 9.602, p<0.001).
Baji
In the front habitat, Baji spent the least amount of time in the area near the
barrier to the lower habitat (16.67% +/- 2.45%). He increased his time near the
barrier to the back habitat with the change in rotation (1st rotation: 19% +/-
4.62%; 2nd rotation: 37.73% +/- 6.39%). In the back habitat, regardless of
rotation he spent the most time by the barrier to the front habitat (56.42 +/-
5.40%). He spent the least amount of time in the middle area of the habitat
(13.25% +/- 2.92%). In the lower habitat, Baji spent just under half his time in
the third of the exhibit located by the back habitat (47.38% +/- 5.01%). Baji
also spent 21.98% (+/- 3.65%) of his time near the barrier to the front habitat
regardless of rotation.
Baji consistently spent a large portion of his time out on the cement (front
habitat: 74.28% +/- 5.79%; back habitat: 51.38% +/- 6.62%), even in the lower
habitat. When in the lower habitat he spent similar amounts of time on the
cement (37.94% +/- 4.59%) and the dirt (36.51% +/- 4.53%). The most time he
spent in resting areas was in the back habitat (plastic culvert: 46.34% +/-
6.87%; nest box: 0.89% +/- 0.31%). However, he did spend roughly a quarter
of his time in resting areas in the other two habitats (front habitat, nest box:
25.08% +/- 5.80%; lower habitat, plastic culvert: (25.48% +/- 6.31%). He was
rarely seen in the boxes with pine shavings (front habitat: 0.63% +/- 0.23%;
back habitat: 1.38% +/- 0.64%).
Baji exhibited more time locomoting (F2,118 = 7.201, p = 0.001) and less
time resting (F2,118 = 4.401, p = 0.014) in the front habitat compared to the
back and lower habitats. Baji also showed a significant increase in pacing in
the front habitat compared to the lower habitat. On average, he spent 13.8%
(+/- 2.49%) of his activity budget engaged in this pursuit in the front habitat,
but only 5.5% (+/-1.72%) and 8.8% (+/-2.66) of his time engaged in a similar
fashion in the lower and back habitats, respectively. There was no significant
difference in the amount of pacing observed between the back and front
habitats and the back and lower habitats.
While there was no significant effect of rotation on locomotion (F1,118 =
0.642, p = 0.425) and resting (F1,118 = 3.353, p = 0.070), Baji showed a trend
towards pacing more in the second rotation than the first. There was also a
difference in how pacing was affected by the impact of rotation on housing
condition. In the first rotation, there was no significant difference in amount of

pacing between housing conditions. In the second rotation, there was a
significant increase of pacing in the front habitat compared to the lower
habitat. There were no significant differences between the back habitat and the
front or the lower habitat. In addition, there was an interaction of housing
condition and rotation found with the resting behavior (F2,118 = 4.433, p =
0.014; Figure 7), as Baji was more likely to rest in the front habitat during the
first rotation than the second; however, rotation did not affect his resting
behaviors in the other two habitats.
There were no significant effects (housing condition: F2,118 = 1.069, p =
0.347; rotation: F1,118 = 2.770, p = 0.099) or interaction between housing
condition and rotation (F2,118 = 0.548, p = 0.579) for the exploring behavior. In
addition, there was no interaction for housing condition and rotation for
locomotion (F2,118 = 1.341, p = 0.266).
The effect of the implant was not significant for all behaviors
(locomotion: F1,118 = 2.346, p = 0.128; rest: F1,118 = 1.354, p = 0.247;
exploration: F1,118 = 0.329, p=0.567) except pacing. Baji showed a trend to
pacing more after his implant compared to before (U = 1198.00, p = 0.051).
Figure 7. Interaction of housing condition and rotation on the time Baji spent resting.
Error bars represent SE and (*) indicates p < 0.05 for pairwise comparisons in a
generalized linear mixed model.
Time near shared barriers showed no main effect for rotation (F1,118 =
0.739, p = 0.392), presence of the implant (F1,118 = 0.370, p =0.544), or an
interaction between housing condition and rotation (F2,118 = 1.112, p = 0.332),
but there was an effect of housing condition (F2,118 = 4.976, p = 0.008) where
Baji spent more time near barriers in the front habitat compared to the lower
and back habitats.
Biological Validation of FGM Assay for Aardvarks

FGM concentrations in fecals collected the day after veterinary exams
were elevated more than two standard deviations above baseline for both Baji
(baseline mean + SD = 735.8 + 281.2 ng/g dry feces) and Roxaane (baseline
mean + SD = 370.6 + 57.7 ng/g dry feces) but did not show a trend for Kaatie
(Figure 8). FGM concentrations increased by 198.9% for Baji compared to
baseline after the exam, while concentrations for Roxaane increased by
560.0%. Fecal FGM concentration remained elevated for Baji two days after
the exam but had returned to baseline by the fourth day (the day three sample
was not available), while concentrations returned to baseline the third day after
the exam for Roxaane (the day two sample was not available).
2500 a
2000
1500
1000
500
0
-5 -3 -2 0 1 2 4 5
Days from Vet Exam
3000
b
2500
2000
1500
1000
500
0
-4 -3 -1 0 1 3 4
Days from Vet Exam
Figure 8. FGM concentrations measured in response to a regularly scheduled

veterinary exam for an adult male and an adult female aardvark, Baji (a) and Roxaane
(b). The solid horizontal lines indicate mean baseline concentrations, and the dashed
horizontal lines indicated the baseline mean + two standard deviations.
Analysis of FGM by Housing Condition

For all aardvarks except Rachaael, for whom fecal samples were not
available during the first rotation, FGM concentrations were significantly
associated with rotation (F1,190 = 33.06, p < 0.001) and habitat as a function of
rotation (F2,190 = 5.01, p = 0.01), but not habitat alone (F2,190 = 1.13, p = 0.33).
FGM concentrations were significantly lower during the first rotation
compared to the second (t17 = -4.65, p < 0.001). Differences between habitats
were evident during the second rotation but not the first. During the second
rotation, FGM concentrations were higher in the lower habitat compared to
both the front (t104 = 2.57, p = 0.01) and back habitats (t101 = 2.62, p = 0.01),
while the front and back habitats did not differ from one another (t190 = 0.13, p
= 0.90).
Figure 9. Fecal glucocorticoid metabolite concentrations (FGM; mean + SE) for

aardvarks Baji (a) and Roxaane (b) in three different housing spaces during two
different rotations that impacted nearest neighbor designations. (*) indicates p < 0.05
for pairwise comparisons in a generalized linear mixed model.
Baji (Figure 9a) had significantly higher FGM concentrations during the
second rotation (F1,68 = 9.70, p = 0.003) and after receiving the implant (F1,68 =
22.84, p < 0.001), periods with substantial overlap. The effects of habitat (F2,68
= 3.55, p = 0.03) were also significant but dependent on rotation (F2,68 = 2.73,
p = 0.07). FGM concentrations were higher overall for Baji in the front
compared to the back habitat (t68 = 2.61, p = 0.01) when the two rotations were
averaged; however, Baji showed the lowest FGM concentrations measured in
any condition in the lower habitat during the first rotation and the highest
overall in the lower habitat during the second rotation. FGM values during the
second rotation were significantly higher in the lower habitat compared to the
back (t68 = 2.33, p = 0.023) and in the front compared to the back (t68 = 2.56, p
= 0.01).
For Kaatie FGM concentrations were significantly lower during the first
rotation than the second (F1,53 = 8.41, p = 0.005). FGM concentrations did not
vary on the basis of habitat (F1,53 = 0.59, p = 0.44) or the interaction of habitat
and rotation (F1,53 = 2.30, p = 0.13). However, there were no samples collected
for Kaatie in the lower habitat, so the habitat comparison was based only on
the front and back habitats.
Because there were no fecal samples collected from Rachaael during the
first rotation, the model included only housing as a fixed factor and showed no
significant differences in FGM concentrations between the different habitats
(F1,22 = 1.1, p = 0.3).
For Roxaane (Figure 9b), FGM concentrations did not vary by habitat
(F2,60 = 2.25, p = 0.11) but approached significance for rotation (F1,60 = 3.83, p
= 0.055) and the interaction of habitat and rotation (F2,60 = 3.0, p = 0.06). FGM
concentrations were generally lower in the first rotation compared to the
second. During the second rotation, FGM concentrations were significantly
higher in the back habitat compared to the front (t60 = 2.87, p = 0.006).
Correlations between Behavior and FGM Concentrations

Pacing totals were positively correlated with daily FGM concentrations
across aardvarks, ( = 0.15, p = 0.02). Higher totals for exploring showed a
trend towards association with lower FGM concentrations ( = -0.1, p = 0.1).
Resting ( = 0.01, p = 0.9) and locomotion ( = 0.08, p = 0.3) were not
correlated with FGM concentrations.
Conclusion
The aardvarks in this study demonstrated differences in their behaviors

and use of space as a factor of housing condition, including location and
neighbor identity. As a group, they were more active in the space with the
largest concrete area (not including pacing), which was somewhat surprising
as the space containing dirt as a substrate could offer them more opportunities
for species-typical behaviors. In a study of blue foxes, Koistinen et al. (2008)
found that foxes preferred mesh areas over dirt areas, and hypothesized that
this could be due to dirt areas being more soiled. As the aardvarks often
defecate in the dirt area, a similar aversion to spending time there may have
occurred. They did tend to pace less often in that space, suggesting that access
to more substrates might play a part in reducing this type of stereotypic
behavior in aardvarks. In a multi-institutional study of another fossorial
mammal, zoo-housed armadillos (Tolypeutes matcus, Chaetophractus
vellerosus, and Dasypus novemcinctus), substrate depth in enclosures was
negatively correlated with both rates of undesirable behavior (predominantly
pacing) as well as FGM concentrations (Baird et al., 2016). More naturalistic
habitats are believed to be more conducive to good welfare as they provide the
resources animals should have to meet their main needs (Fabregas et al.,
2011). The importance of natural features should therefore not be discounted.
The lower habitat was also the space that offered the least amount of access to
aardvarks in adjacent habitats, and more separation from conspecifics in this
solitary species may have impacted their behavior.
Rotation order was changed halfway through the study to determine if
neighbor identity impacted behavior, particularly in the adult male. As a
group, the aardvarks spent more time locomoting during the first half of the
study, suggesting that a change in routine may impact their activity levels. The
group substituted this with increased rest during the second rotation; although
this was not a significant increase possibly due to the effect of housing
condition. Examining the interaction between housing condition and rotation
reveals significant differences in time spent near barriers and pacing for the
aardvarks. They spent more time near the shared barriers when in the front
habitat after the rotation order was changed and less time near the shared
barrier when in the back habitat. This suggests that neighbor identity could be
a factor in use of space for these aardvarks. However, the front habitat did
contain two shared barriers and the back only one. During both rotations, the
aardvarks paced the least in the habitat containing dirt, but there was a
significant increase in pacing in the front habitat after the rotation was
changed. This again suggests a potential influence of neighbor identity on the

behavior of the aardvarks. Aardvarks rely heavily on olfaction, and it is
important to consider their sensory ecology in regards to their physical and
social environment (Newberry, 1995). Their behavior may be impacted by the
presence of conspecifics within their sensory range.
Individual results varied, supporting the concept that welfare is
experienced and thus should be measured on the level of the individual.
Rachaael, the oldest female who was socially housed with her youngest
daughter, showed the least amounts of active behaviors in the back habitat,
which was the smallest in size. However, this is also the space in which she
paced the most. As Rachaael is socially housed, the smaller space may be
more restrictive for her as she is in closer proximity to the daughter with
whom she shares the space. Social density has been shown to impact behavior
and welfare (see Morgan & Tromborg, 2008). As aardvarks are naturally
solitary, being housed socially may impact both of these individuals. Although
switching the rotation order did not alter Rachaael’s overall activity budget,
time allocated to locomotor and exploratory behaviors within each habitat
differed between the two rotations. Rachaael spent less time locomoting in the
back stall during the second rotation compared to the first, and she spent more
time exploring in the front and lower habitats when compared to the back
habitat during that time as well. Although Rachaael did not show an overall
effect of rotation change on resting behavior, her time spent in nest boxes,
which are primarily used to rest, decreased during the second rotation.
Trends in use of space for Rachaael also provide some possible insights
into social preferences for this largely solitary species. Rachaael’s time spent
near the shared barrier when she was in the back habitat decreased
significantly in the second rotation. During the first rotation, she shared that
barrier with her older daughter (Roxaane), and during the second rotation, that
barrier was shared with the adult male (Baji). When she was housed in the
front habitat during the second rotation, Rachaael also showed a 5% increase
in time spent near the barrier to the back, which gave her access to Roxaane,
compared to during the first rotation when that barrier would have given her
access to Baji. Social behavior is poorly studied in free-ranging aardvarks, but
female offspring are thought to stay with the mother longer than male
offspring (Rahm, 1972). Thus, perhaps for this largely solitary species, access
to same-sex and/or related individuals is preferred over access to mating
partners. An examination of how much of their habitat each aardvark used
demonstrated that Rachaael did not use each habitat equally and in each case
spent almost half of her time in one section, and the particular area changed
for two of the habitats after the switch in rotation. Interestingly, for the front
habitat, this area always remained away from both shared barriers.
Kaatie, who was socially housed with her mother Rachaael, also paced
more in the back habitat than the other two spaces. Her overall activity levels
decreased during the second rotation, including a reduction in time spent
pacing. As this behavior was already occurring at very low rates, it was almost
entirely extinguished during the second rotation. Pacing is often considered a
negative welfare indicator, and Kaatie did not seem to experience this
response, although the lowered rates of active behavior may reflect a change in
her welfare status. Increased inactivity has been linked in some cases to
negative affective states, but more research is needed to better ascertain the
true meaning of this behavioral response (Fureix & Meagher, 2015). It is
possible that in her case, a change in routine suppressed her activity levels, but
firm conclusions on any welfare impact are unclear at this time. Kaatie also
spent significantly more time near a shared barrier when she was housed in the
front habitat, regardless of rotation order. This habitat shares a barrier with
both of the others, and this could account for the difference. As the youngest
of the aardvarks, she may have sought out more opportunities for social
interactions. Kaatie also preferentially spent time in specific sections of each
habitat, and these preferences corresponded with those of her mother. She also
used the plastic culverts more during the second rotation, which like the nest
boxes were primarily used to rest, and which corresponds with her overall
decrease in activity levels.
Roxaane was most active in the front habitat, including higher levels of
pacing. The change in rotation revealed that she reduced her time spent
locomoting and exploring in the lower habitat and increased levels of both in
the back habitat. Roxaane spent significantly less time near the shared barrier
in the lower habitat, which is contrary to the other three aardvarks who showed
no change in time spent by the shared barrier in the lower habitat.
Interestingly, she spent less time near the barrier she shared with the male
aardvark than she did near those she shared with her mother and sister and this
may account for the change in time spent near the barrier to the lower habitat.
Roxaane spent more time in the same habitat areas as the other aardvarks
except in the front habitat where she spent the majority of her time near the
shared barrier to the lower stall. The preferential nature of this space is
unknown as the only aardvark that spent a substantial amount time at the
shared barrier when in the lower habitat was the male aardvark. This area also
led to the keeper hallway and to the outside habitat; however, the majority of
the observations occurred while it was too cold for the aardvarks to spend time
outdoors. Finally, Roxaane decreased her time spent in plastic culverts after
the rotation switch and increased her use of the dirt substrate. The reason
behind this preference change is also unknown at this time.
Baji, like Roxaane, had higher activity levels in the front habitat and paced
more in that space than he did in the lower habitat. This was driven by lower
levels of resting and higher levels of pacing in the front habitat specifically
during the second rotation, potentially due to the location of the co-housed
females, or due to a disruption in his routine. He was also the individual who
exhibited pacing behavior the most frequently, although at still relatively low
rates. Both proximity to conspecifics (Bashaw, 2000) and separation from
them (see Mason & Rushen, 2006) have been found to increase pacing in a
number of different species. In Baji’s case, the inability to be with the females
may have led to this behavior being more prevalent. Baji also spent more time
near shared barriers when he was housed in the front habitat, possibly due to
increased potential social interactions. Baji was also seen to pace more after he
received the Deslorelin implants, a behavior that was hoped would decrease as
a result of the hormone regulation. Pacing was positively correlated with FGM
concentrations, and it is possible that both were influenced by the implants
rather than directly causally related to one another. Testosterone and some
behavior levels have been reduced using this type of implant in other species
(zebra finches: Murphy et al., 2015; carnivores: Bertschinger et al., 2000). If
Baji’s behavior was driven by reproductive urges, chemically reducing
testosterone could have decreased pacing. However, this type of GnRH
antagonist has not been used in this species before, and therefore the effect of
this intervention were not certain. Additionally, we only observed Baji for four
weeks post-implantation, and changes in his behavior may have occurred after
the observations ended. Baji’s location preferences matched those of the co-
housed females, but the rotation change resulted in a switch in his preference
for the area with the large shared barrier after the rotation. During this rotation,
that location was closest to the habitat with the co-housed females.
For three of the aardvarks, FGM concentrations were significantly lower
during the first rotation, especially in the lower habitat. This could be due to a
combination of factors including access to dirt substrate, a well-established
housing routine, and/or the impact of neighbor identity. Exposure to new
situations can increase adrenocortical activity (Mason, 1968). Thus the change
in routine may have impacted their FGM concentrations. For all aardvarks,
pacing and FGM concentrations were positively correlated, and as locomotion
was not correlated with FGM concentrations, this may demonstrate that FGM
concentrations may be indicative of a stress response in this species.
Exploration and FGM concentrations did trend towards a negative

relationship, suggesting that situations that encourage such behavior may
reduce stress in aardvarks. Exploration has been cited as an indicator of
positive welfare (Witham & Wielebnowski, 2013), and increasing
opportunities for such behavior should be a goal for the aardvarks.
Examining these results at the level of the individual shows that
Rachaael’s FGM concentrations did not differ between habitats. Although no
comparisons can be made between rotations, it may be that access to specific
environmental features and social opportunities do not cause a change in her
stress response.
Kaatie only showed a difference in her FGM concentrations between
rotation, which may reflect an effect of changes in routine for this individual.
Roxaane also had lower FGM concentrations during the first rotation, although
she did have higher concentrations in the front habitat when compared to the
other two during the first rotation. As this was the habitat in which she was
most active and paced the most, this is not surprising.
Baji had higher FGM concentrations both during the second rotation and
after being implanted, but these co-occurred which could have confounded the
results. In his case, he had his lowest concentrations in the lower habitat
during the first rotation and the highest in the same habitat during the second
rotation. This habitat has the smallest shared barrier and perhaps social access,
or lack thereof, had an impact on his HPA-axis activation.
These results provide quantitative information that may assist with making
evidence-based management decisions for the aardvarks residing at the Detroit
Zoo. Analyzing use of space can help to assess how appropriate captive
environments are (Ross et al., 2009) and physical feature preferences can also
help to guide habitat design (Ross & Lukas, 2006). The low use of the dirt
substrate has led to the determination that despite this being a potentially
beneficial area for species-typical behaviors such as digging, it is not serving
the intended purpose. The dirt has since been replaced with a type that may
allow for more digging and burrowing. The shared barriers, which impacted
the individual aardvarks differently, could also be modified. The results of this
project showed that the aardvarks had individual preferences for certain
features in their environment, which has been demonstrated in other species as
well (Ross et al., 2009). Although the aardvarks did not perform high levels of
pacing, the male did show an increase in this behavior during the second
rotation and after receiving Deslorelin implants. The increase seen in Baji’s
pacing led to a return to the original rotation order, and further data collection
will enable us to determine if this results in a decrease in this behavior, or if
the implant potentially has a longer-lasting effect. Additionally, this study has
revealed activity patterns for each of the four aardvarks and their individual
behavioral diversity. As range of behaviors can be an indicator of welfare
(Miller et al., 2016), monitoring activity budgets is one way to assess the
wellbeing of individual animals.
Overall Conclusion
The results of these studies highlight the importance of assessing welfare

at the level of the individual. Welfare is experienced by individuals, and it is
not surprising that individual drills, gorillas and aardvarks responded
differently to particular situations. It is important to evaluate practices and
habitats to ensure that decisions are made based on evidence rather than
assumptions, even those based on species natural history, and are having the
intended impacts. A scientific approach to providing for welfare has been
encouraged (Hill & Broom, 2009), and systematic evaluations such as these
can add to our understanding of the needs of individuals of various species,
which is lacking in many cases (Fidgett et al., 2008). Welfare ranges on a
continuum from poor to good, and an individual’s status can and does change
over time. Conducting evaluations on an ongoing basis to capture these
differences and to address them in a timely manner should there be a need is
also important.
Welfare assessments, and the potential solutions to welfare questions are
not one-size fits all. Although we continue to apply scientific methodology to
evaluate animal welfare, innovation is critical if we are to be successful in
ensuring each animal living in the care of humans is thriving. Each type of
methodology has strengths and weaknesses, and should be validated on a case
by case basis to ensure that the most accurate information will result. A
combination of behavioral observations in conjunction with hormone
monitoring is widely used and in the case of the aardvark project was an
effective way of obtaining data to better understand how the aardvarks were
spending their time and how that was impacted by their location, as well as the
identity of their neighbors. As their active period occurs when staff responsible
for their care are not present, this type of information can be incredibly helpful
when making decisions that not only improve basic care, but address their
overall welfare as well. The use of keeper questionnaires was a less effective
way of assessing the impact of night-time housing for drills and gorillas.
Although keepers had originally reported a difference in the gorillas based on
where they spent the night, this was largely not reflected in their ratings. It is
important to carefully refine and validate data collection strategies, and in the
case of welfare assessments, to utilize multiple measures (Hill & Broom,
2009; Swaisgood, 2007).
Most importantly, these studies underscore the importance of considering
the welfare of individual animals over the course of entire days. Zoos provide
homes for numerous species, all of which have different needs, and those
needs can and do vary by individual. Examining management decisions that
impact animals when assessment is less easily achieved can prevent or modify
situations that are less conducive to good welfare. Diurnal species may be
more active during day-time hours, but their overnight hours are also critical
and must not be discounted when evaluating how animals are faring overall.
Nocturnal species provide additional challenges, as their activity patterns are
less easily discernable by their primary caregivers. Measures must be taken to
understand the impact that their environment, both physical and social, has on
them. Zoos can at times be challenging places in which to conduct research, as
control over various aspects may not be feasible (Swaisgood, 2007). They are
also places that must be dedicated to providing each animal living in them
with experiences that promote good welfare at all times. Commitment to
systematic monitoring and evidence-based management enhances such efforts
and brings the zoo community closer to being animal welfare centers.
ACKNOWLEDGMENTS
The authors would like to thank the Detroit Zoological Society primate
and night staff for their assistance with the projects, the Center for Zoo Animal
Welfare interns, residents and volunteers who assisted with data collection, the
volunteers who helped with processing samples in the endocrinology lab and
the Detroit Zoological Society for supporting our work.
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BIOGRAPHICAL SKETCH
Stephanie Allard
Affiliation: Detroit Zoological Society

Education: Ph.D. in psychology, Georgia Institute of Technology
Business Address: 8450 W. 10 Mile Road, Royal Oak, MI 48067
Chapter 2
AN INTEGRATIVE APPROACH TO
REALIZING ANIMAL WELFARE - ETHICS,
ENVIRONMENT AND SCIENCE
Ryunosuke Kikuchi1,2,,
Rosário Plácido Roberto da Costa1,3
and Myriam Kanoun-Boulé1
1
CERNAS/Escola Superior Agrária, Politécnico de Coimbra, Portugal
2
Faculty of Science and Technology, Ryukoku University, Japan
3
Departamento de Ciências Zootécnicas/Escola Superior Agrária,
Politécnico de Coimbra, Portugal
ABSTRACT
Animal welfare has become an important issue in recent years. There
is an increasing interest in animal welfare in many countries.
Urbanization, the influence of the media and civil society organizations,
and higher levels of education are reasons for an increased interest in
animal welfare. Consideration of animal welfare should encompass not
only the physical health but also the psychological well-being of animals.
The term ‘welfare’ defines the state in which a person or animal lives
healthily, happily and safely. The subject of animal welfare is discussed

Corresponding author: kikuchi@esac.pt.
56 R. Kikuchi, R. P. Roberto da Costa and M. Kanoun-Boulé
from the viewpoints of cruelty (ethics), conservation of wild animals

(environment) and veterinary attention (science).
The majority of people believe that animals are currently raised
without cruel treatment, but reports of animal cruelty are not unknown:
for example, bear farming typically entails the imprisonment of bears in
squeeze cages for years; a catheter is inserted daily into a bear’s gall
bladder or a tube is implanted internally in order to collect dripped bile;
workers often mutilate the bears by breaking their teeth and pulling out
claws for the sake of human safety; and when the bears cannot produce
sufficient bile, they are left to die of starvation or are killed for their parts.
Habitat loss, climate change, poaching, and pollution paint a bleak
picture for threatened and endangered species around the world. It is
estimated that about 10,000 species annually become extinct. This rapid
extinction is happening through the trade in at-risk species, expanding
cities which destroy habitats, the conversion of fertile wildlife land
habitat for agriculture or pastures and human-driven changes. Directly or
indirectly, human society has multiple impacts on wild animals’ welfare
and survival. Natural reserves, protected areas and rehabilitation centers
for threatened wildlife are some of the possible ways to counterbalance
our footprint on wild fauna and to promote protection and conservation.
However, if international policies are essential for starting and moving
towards a standard concept of animal welfare, effective realization of this
concept can be achieved only through keen environmental awareness by
citizens around the globe.
The veterinary profession is privileged to occupy a position of
enormous social influence on animal welfare issues. However, the
profession has traditionally understood welfare primarily within the
limited scope of animal health and productivity. Currently, animal
welfare focuses on companion and farm animals, and welfare during
transport of the animals and at slaughter, but a greater emphasis must be
placed on the welfare of wild animals in captivity or conservational parks
and those animals that have lost their natural habitats.
The importance of animal welfare differs from country to country
owing to differences in religion, economic development, education and
perception. Animal welfare is not restricted to a single field: it is a subject
that interests both scientists and the public. Although it is not enough to
discuss only one aspect of animal welfare, an integrative approach is may
be necessary to describe the concept of animal welfare.
1. INTRODUCTION
Animal welfare has become an important issue in recent years ‒ there is an
increasing interest in animal welfare in many countries (review in (Koknaroglu
An Integrative Approach to Realizing Animal Welfare 57
and Stoklosa, 2013)). Urbanisation, the influence of the media and civil
society organisations, higher levels of education and economic advances are
reasons for an increased interest in animal welfare.
Consideration of animal welfare should encompass not only the physical
health but also the psychological well-being of animals. The term “welfare”
defines the state in which a person or animal lives healthily, happily and safely
(Wehmeier, 2005). There are other definitions of animal welfare: for example,
a state of complete mental and physical health, where the animal is in harmony
with its environment (Hughes, 1976); and living or adaptation of animals
without suffering in the environments provided by man (Carpenter, 1980). In
discussions of animal welfare, it would not be enough to talk only about
environmental conditions. Based on the above-mentioned definitions, animal
welfare can be defined as providing environmental conditions in which
animals can display all their natural behaviors. The importance of animal
welfare differs from country to country owing to differences in religion,
economic development, education and perception. Animal welfare is not
simply a topic of interest on farms: it also interests scientists and the public.
However, there is no animal welfare regulation that can be applied to all
countries (review in (Koknaroglu and Stoklosa, 2013)). Animal welfare laws
and rules have matured over the last 200 years, and treating animals badly is
now referred to as cruelty (Rollin, 1999). A statement regarding animal
welfare was agreed in the Amsterdam Treaty by the European Union member
states in June 1997 which was officially signed on 2 October 1997 and entered
into force on 1 May 1999. The European Farm Animal Welfare Council
adopted rules relating to five freedoms of animals which define ideal states
rather than standards for acceptable welfare. These are freedom from hunger
and thirst; freedom from discomfort; freedom from pain, injury and disease
through prevention or rapid treatment; freedom to express normal behavior
through the provision of adequate space and facilities, and company of the
animal’s own kind; and freedom from fear and distress through the provision
of conditions and treatment which avoid mental suffering (review in (Cox,
2009)). The dimensions of welfare and their inextricable relationships are
illustrated in Figure 1.
It follows from Figure 1 that studies on animal welfare are scientific in
nature, and they conceptually overlap with rules and applications that are
based on ethical perception. To put it differently, animal welfare is not just the
absence of cruelty or unnecessary suffering. It is much more complex;
therefore, the subject of animal welfare is discussed from the viewpoints of
cruelty (ethics), conservation of wild animals (environment) and veterinary

attention (science) in this chapter.
Figure 1. Concept of animal welfare proposed by the World Society for the Protection
of Animals (redrawn from (Cox, 2009)): animal welfare is traditionally centered on the
physical state; mental states are becoming increasingly understood and explored; and
naturalness refers to the ability of the animal to fulfill its natural needs.
2. CRUELTY - A CASE STUDY OF BILE EXTRACTION

FROM BEARS
The majority of people believe that animals are currently raised without
cruel treatment, but reports of animal cruelty are not unknown; examples
include entertainment such as bear baiting, inhumane killing, and live trade
(WSPA, 2010). This subject is discussed on the basis of an Asian case study.
2.1. Animal-Based Traditional Medicines
Traditional Asian medicine is a holistic approach to healthcare where

patients are treated using natural plant, mineral, and animal-based ingredients
(cf. Ellis, 2005). Figure 2 is discussed on the basis of a case study. This
medicine dates back at least 3,000 years and is an indispensable part of
Chinese cultural heritage (cf. Ellis, 2005).
The Chinese pharmacopeia frequently relies on medicines made from
animals that are rumored to have curative properties, and these medicines
include not only bears but also other animals (cf. Ellis, 2005); for example,
elephant skin is taken for acne, monkey heads are eaten for headaches, tiger
bones are taken for human virility and their whiskers are consumed for
toothaches (Figure 2A), ground rhino horn is used to cure almost every disease
Figure 2B), snake glands are good for the eyes, turtle heads are consumed for
labor pain, and lizards are taken for high blood pressure.
Figure 2. Animals used for traditional Asian medicine (courtesy Facts & Details
Project): (A) a tiger amputated for the Asian tiger medicine and product market ‒ with
Asians’ rising incomes, people today can afford expensive tiger medicines, which has
created more demand (Ellis, 2005); and (B) a rhino is killed for its horn – in certain
Asian countries, ground rhino horn is used to cure almost every disease (Ellis, 2005).
2.2. Captive Bears on Asian Bear Farms
Bear bile is used in fighting fever, detoxification, and reducing

inflammation, swelling, and pain (Feng et al., 2009). The number of captive
bears is roughly estimated at about 13,000 in Asia (review in (Kikuchi, 2010)):
about 7,000 Asiatic black bears are legally kept on China’s farms for bile
extraction – cf. the number of illegal captive bears in China is unknown; about
2,000 Asiatic black bears are legally kept on Korea’s farms for propagation;
and about 4,000 bears (Asiatic black bears and Malayan sun bears) are
illegally kept on Viet Nam’s farms for bile extraction.
The production of bear bile in China rose from about 500 kℓ in the 1970s
to about 7,000 kℓ in the late 1990s. The oversupply of bear bile is used in
products with no medical purpose such as shampoos, creams, etc.(BBC,
2006).
2.3. Bile Extraction from a Living Bear
Though bear cubs stay with their mothers for 2–3 years in the wild, cubs
born on farms are taken away from their mothers when they are 2–3 months
old, and the cubs are then taught a range of circus-type tricks such as standing
on their hind legs, handstands, carrying chairs and so on in order to provide an
attraction (e.g., petting and photography) for farm visitors and play a role in
marketing bile products (WSPA, 2005). Such attraction seems to provide
additional revenue for the bear farming industry, but the performing life of a
bear cub is short and may only last until it is about 2 years old (WSPA, 2005).
Once a bear reaches about 2.5 years old, it is used for bile extraction. Over
a long period of captivity for bile extraction, the adult bears are kept in cages
little bigger than their own bodies (see Figure 3A), so they are often hurt from
rubbing or hitting themselves against the iron bars of their tiny enclosures
(WSPA, 2005). The bears are fed various mixtures such as rice, vegetables,
cereals, and fishmeal twice a day. Instead of free access to water, most farms
only hose the bears down once a day (WSPA, 2005).
The bile extraction is generally carried out in a bear’s permanent living
cage that provides insufficient space for the bear’s movements. The bears are
fed twice a day to stimulate bile production. On most farms, the feeding tray is
attached to the cage below the bear’s chin because this forces bears to scrape
the food into their cages while lying on their stomachs, which facilitates bile
extraction (see Figure 3B). Bile extraction is surgically carried out without
anesthetics by farm workers who have no veterinary experience in many cases
(WSPA, 2005). The bears are kept in cages that are too small to allow
movement, and this immobility enables easy access to the bear’s abdomen;
thus, the painful extraction of bile is performed without difficulty. During the
bile extraction, the bears twitch, gnash their teeth, bite the bars, and utter
distress calls; they curl up after the extraction, shiver, and hold their paws to
their stomachs. Bears can perceive terror and feel pain the same as we
humankind do (IUCN, 2007). The above-mentioned behavioral signs therefore
prove that bile extraction is an extremely painful procedure. As stated above,
bears can perceive terror. This suggests that farm workers engaged in bile
extraction need to approach the bears without fear of injury (i.e., the reduction
of danger); hence, farm workers often subjugate and mutilate the bears by
breaking their teeth (see Figure 3C), pulling out claws, and sometimes
removing whole digits.
Figure 3. Asian bear farming for bile extraction (courtesy WSPA): (A) a bear kept
captive for bile extraction spends most (about 10 years) of its life in the cage; (B) farm
workers extract bile from the gall bladder; and (C) broken teeth (upper picture) and
open tooth roots (lower picture) can be constantly painful because the nerve inside the
tooth may be damaged and exposed to the air, food and water.
The free-dripping technique has been encouraged by the Chinese

government since the mid-1990s (Loeffler et al., 2007): (i) after each fistula
(hole) is made in the abdominal wall and gall bladder, a connection tube is
positioned to link these holes; (ii) this connection tube is fashioned out of
tissue taken from the bear’s abdomen; and (iii) when a farm worker inserts a
rubber or steel tube into the hole, bile drips from the hole to a tray or is drawn
out with a syringe. However, the wound (hole) is vulnerable to infection, and
the caustic nature of bile causes chronic irritation and ulceration on the skin,
resulting in a high mortality rate (Loeffler et al., 2007). The other problem lies
in bears’ good healing capacity – that is, bears’ wounds heal quickly (WSPA,
2005). The fistula (wound) heals spontaneously, so a farm worker must force a
catheter through the healing tissue in order to extract bile. If the hole closes up,
a red-hot steel catheter is often inserted to re-open the wound without the use
of anesthetics. This severe pain must be unimaginable.
In order to overcome the difficulty of maintaining the fistulas (holes), the
so-called fake technique has been applied since 2005 (Loeffler et al., 2007). A
perspex catheter is positioned in the gall bladder, and the external end of this
catheter is cut just beneath the abdominal skin. There is a bulb at the internal
end of the catheter, and this bulb prevents the catheter from falling out from
the gall bladder; moreover, this catheter is fixed with wire flanges that jut into
the tissue between the gall bladder and the abdominal aperture. During the use
of the fake technique, the wall of the gall bladder becomes thicker, its mucosa
is congested with polyps, the tissue surrounding the fistula is infected, and
abscesses form around the wire flanges (Loeffler et al., 2007).
When a bear can no longer produce sufficient bile, the bear is normally
moved to another cage (i) to await death through major sickness such as
cholecystitis, cholelithiasis, polyp formation, or liver cancer (Loeffler et al.,
2007); (ii) to be killed for its paws and gall bladder (WSPA, 2005) ‒ if
customers of the bear farm so require, bear paws are cut off because the paws
are eaten as a delicacy in Asia (China and South East Asia in particular) and
the sale of bear parts provides an additional income for farms; or (iii) to be left
to die of starvation.
Thus, it can be concluded that bile extraction from living bears is the
worst scenario in terms of animal welfare.
3. WELFARE OF FREE-LIVING WILD ANIMALS

Anthropogenic threats to wild animals’ welfare greatly increased during
the last century and many wild animal species are likely to become extinct due
to impacts of recent human activities on the environment unless there is
conservation action (e.g., habitat protection and management, captive breeding,
translocation) (McNeely, 1992; Heywood et al., 1994; Magin et al., 1994;
Kirkwood and Best, 1998; WWF, 2016).
Whether as free-living or short-term residents in a rehabilitation center,
wild animals can feel pain and distress owing to direct or indirect human
intervention. When focussing on the individual animal, from the veterinarian
approach, wild animal welfare is more based on physical and mental
functionings as well as behavioural aspects while, in a conservationist
framework the emphasis is given to the welfare of the whole species and the
preservation of the ecosystem. However, ultimately both approaches prove to
be two complementary issues of the same concern.
Thus, wildlife medicine, which has seen growing interest and great
advances over the last 20 years and which aims to control wildlife diseases
and/or to rescue and rehabilitate wild animal casualties, is generally
undertaken for conservation purposes, protecting or promoting the
preservation of threatened species, as well as for improving the welfare of
individuals (Kirkwood and Sainsbury, 1996). The application of vaccination
programmes to free-living populations of endangered species to protect them
from infectious diseases which might threaten their survival is one example
among many others of wildlife medicine applied in a wide conservation
approach (Sholley, 1989; Rupprecht et al., 1990; Gascoyne et al., 1993).
3.1. Anthropogenic Impact on Free-Living Wildlife Welfare
In 2005, Leach and his colleagues carried out a survey ordered by the
World Society for the Protection of Animals to identify priority welfare issues
affecting free-living wildlife in Sub-Saharan Africa and Latin America (Leach
et al., 2005). Other emerging reviews and research in different regions tend to
demonstrate that the same issues also apply to almost all species of free-living
wild animals worldwide (Porter, 1992; Crawford, 1996; Vitousek et al., 1997;
Kirkwood and Best, 1998; Brandão, 2008, 2009; Molina-Lopez et al., 2011).
All threats can be broadly organised into three main categories: trade in free-
living wildlife, hunting and fishing, and human infringement. Although the
two first issues remain important concerns in the 21st century, human
encroachment is by far the most important issue affecting the welfare of free-
living wild animals. Loss of habitat, pollution, human contact and wildlife
management are among the major negative impacts caused by human
infringement.
3.1.1. Habitat Loss

This issue resulting from human activities refers to the destruction,
fragmentation or degradation of the natural habitat where a wild species used
to live (see also Figure 4). Among the major anthropogenic causes of habitat
loss we can identify:
 Expanding urban development which causes wildlife habitat reduction

 The constructions of roads and fences leading to habitat fragmentation
 Mining activities and natural resource exploitation which often induce
a disruption of ecosystem functioning and associated services (e.g.,
water supply)
 The conversion of fertile wildlife land habitat for agriculture and
pastures which generally results in food competition between wild
species and livestock, depletion of natural resources in the case of
grazing or land clearing, and disruption of the balance of the
ecosystem when crops or pastures are cultivated
 Natural or manmade disasters that alter the habitats of the fauna, like
for example, forest fires which devastate the entire ecosystem of the
region leading to deaths and sufferings of the wildlife and livestock.
Figure 4. Habitat loss threatening wildlife animals (redrawn from (Ewing et al., 2005)):
(A) loss of habitat to urbanisation and agriculture are among the greatest threats to the
Florida panther; (B) rapid development along Colorado’s front range has contributed to
a decline in the Preble’s meadow jumping mouse; and (C) the survival of the Canada
lynx requires large tracts of undeveloped forest.
The demand for animal protein is on the rise and, coupled with the
increasing human population in the developing world (see also section 4 of the
present chapter), a solution has to be sought as to how best to meet this
demand as this issue is probably one of the most serious concerns regarding
habitat loss and wildlife welfare. The increase in livestock production means
more land is required for pastures for the animals, for the production of feed
for the animals and for creating new production units. This means that the
more vulnerable group that shares this planet with us – the wildlife – pays a
high price for this. Way back in history the occupation of land by humans for
their benefit brought pressure on the welfare of wild animals (National
Research Council, 1970). For instance, in Africa, the conservation of wildlife
habitat is important for the welfare of animals, but owing to human population
growth and greater demand for land for grazing, cultivation and housing, many
reserves have seen their boundaries diminished and the wildlife labelled as
pests to be eliminated when they pass over cultivated fields (Masiga and
Munya, 2005).
The consequences of habitat loss on the welfare of free-living wildlife
include the distress and suffering the animals will feel owing to a wide range
of disruptions such as the disturbance of breeding and nesting locations;
disruption of natural behaviour and movements (displacements of animals
from their home ranges); alterations of migration routes; fragmentation of
social groups and populations; increased predator vulnerability and inter-
species competitions; and starvation as a consequence of the competition with
livestock for food and water. More directly, animals can feel fear owing to the
proximity of human beings or experience severe pain, injuries or death in the
case of collisions with man-made objects or as a consequence of a deliberate

attempt at extermination when animals are considered as pests or dangerous
(see also the section 3.1.4. Wildlife management).
3.1.2. Environmental Pollution

The environmental problem caused by accidental or deliberate release of
contaminants into the biosphere (air, water and soil) is another serious threat to
the welfare of free-living wild animals. Uncontrolled disposal of household
and industrial rubbish, contamination of the soil by inappropriate disposal of
industrial and household waste and the release of industrial and household
chemicals into the water are the main causes of wild animal injuries and deaths
each year. More indirectly, the release of industrial chemicals into the
atmosphere from industrial processes, power generation, vehicle exhausts (e.g.,
sulfur dioxide and nitrogen oxides) leads to the formation of acid rain and
tropospheric oxidative pollution which affect both animals and their habitats
worldwide. Finally, the excess of heat, sound and light originated from
anthropogenic activities is another source of pollution which greatly affects
wild animal behavior.
3.1.3. Contact and Interaction with Humans and Their

Domestic Animals
The relationship of humans and their domestic animals with wildlife is
another area of concern for the welfare of free-living wild animals caused by
human infringement. In areas where humans and wildlife share the same
habitat, the proximity of humans and domestic animals (companions and
livestock) poses a serious threat to free-living wild animals. The close
proximity between livestock and wildlife in these areas can lead to health
hazards which are linked with the transmission of diseases between animals,
which could, in turn, threaten human health and the welfare of all. The risk of
disease transmission is greater when the means to impose sanitary controls are
insufficient (e.g., in the case of developing countries or in territories that are
suffering conflict situations). However, this situation not only threatens
developing countries but also developed zones. Reference has been made to
the paradigm of this issue and to the different ways of controlling the problem
(Gortazar et al., 2015). Furthermore, companion animals (e.g., cats and dogs)
are known to be serious predators of wildlife (e.g., small mammals and birds)
worldwide, hunting and attacking a wide range of wild species, causing fear,
distress and suffering and strongly contributing to the decrease of some
species. Some human activities which involve direct contact with wildlife such
as nature tourism and research on wild animals, although potentially beneficial

to wildlife, can also present problems regarding individuals’ welfare. Both
poor methods of capturing animals and inadequate management of visit
activities can induce considerable distress and fear and alter the natural
behavior of wild animals owing to the disturbance caused by visitors or by
trapping.
3.1.4. Wildlife Management

Wildlife management is the last but not the least area of concern regarding
free-living wild animal welfare and it is a direct consequence of habitat loss
caused by human infringement. Such impacts as the concentration of wild
species into increasingly restricted territories owing to the expansion of human
activities, the disruption of natural movement patterns, migration routes and
predation caused by fences and roads which fragment habitats, and the
restriction of wild species distribution to confined areas such as natural parks
and reserves foster the risk of overpopulation and/or the risk of disease
propagation. Human interventions are then necessary to control this
phenomenon. The methods to curtail the wildlife population may imply that
the welfare of wildlife could be at risk. In an initial stage, the techniques used
can consist of trapping, transporting and relocating of a part of the targeted
population. However, in more advanced stages, the culling method (after due
head count) could prove to be acceptable if carried out humanely and which
could help in controlling the spread of diseases by wildlife. Other methods like
immunocontraception could be considered as more socially acceptable to
control wildlife population. One such example of wildlife management in the
case of domestic outdoor pig production, both in developed and developing
countries, is the problem of wild boars invading the farms when the female
domestic pigs are in heat. This leads to the organisation of hunting expeditions
where the wild pigs are killed at large with no veterinary inspection, therefore
creating a situation that could potentially lead to the transmission of zoonotic
diseases such as tuberculosis to humans and to the dogs that eat the offal
(Lopes and Borges, 2004). Further other problems with wildlife management
were recently reported with wild pigs in Spain where wild boar culling was
carried out in the suburbs of Madrid to reduce the menace of these animals
entering the city areas; however, the method used (crossbows) was considered
as inhumane by an animal rights group (Burgen, 2016).
All these methods used to control wild animal populations cause
considerable distress, pain and suffering fostering the risk of injuries, disease
transmission and pain during culling, trapping and transport. In addition,
relocated animals can suffer from social isolation, starvation and distress
resulting from relocation to a new habitat where they are more vulnerable to
predation and diseases. In order to minimize the impacts of wildlife
management on wildlife welfare, all methods and techniques used to control
wild animal populations need to be carefully selected and applied with caution.
3.2. Wild Animal Welfare in Rehabilitation Centers
Situated on the fringe of wildlife management and veterinary science,

wildlife rehabilitation has been practiced for many years. Initially volunteer-
based and privately funded, it first appeared in response to individual animals
and concern for human impact on wildlife and was limited to basic and
improvised methods to rescue, treat and return injured or orphaned wild
animals to their native habitat. Although initially controversial (Loftin, 1985;
William, 1990; Kirkwood, 1992; Crawford, 1994; Rosenman, 1996; Frink and
Miller, 1997), the interest in and value of wildlife rehabilitation as an efficient
way to compensate for human impact is now fully recognized as contributing
to wild species conservation and protection.
Indeed, the recovery and subsequent release into the wild of injured
wildlife focuses on improving the welfare of individual wild animals while
compensating for human impact on nature and wildlife (Williams, 1990;
Swingland, 1992; Crawford, 1994; Duke et al., 1998; Frink, 1998; Haas, 1998;
Kirkwood and Best, 1998).
Today the direct benefits of wildlife rehabilitation are multiple and could
be summarized in several topics: (i) wildlife rehabilitation is peculiar in that it
concentrates on the improvement of the welfare of individual animals while,
by the sum of the recovery successes, contributing to the welfare of the
wildlife community and the reinforcement of the natural population after the
release (Redig and Duke, 1995); (ii) rehabilitation also allows the
identification of the causes of morbidity and mortality, thus acting as an
indicator of human disturbances on environmental health (Williams, 1990;
Cox, 1998). It plays an important role in habitat and wildlife conservation by
fostering the implementation of regulatory changes as a consequence of the
identification of the causes of admission (Crawford, 1994; Redig and Duke,
1995; Duke et al., 1998; Sleeman and Clark, 2003). By serving as a means of
education and promoting public awareness of wildlife and environmental
issues, it fosters knowledge, respect and protection of individuals, populations
and habitats (Sewell, 1996; Cox, 1998; Thrune, 1998); and (iii) rehabilitation
is an important tool for increasing scientific knowledge on wild animals in

diverse areas such as behavior, physiology and nutrition (Thrune, 1998), and
rehabilitation strongly contributes to the conservation of wild species
populations (Swingland, 1992; Duke et al., 1998; Frink, 1998) while providing
opportunities for training wildlife researchers and veterinarians (Porter, 1992;
Seller, 1996).
From the point of view of wildlife natural selection, humans have become
the main selection pressure and the majority of individual animals treated in
rehabilitation centers are casualties of anthropogenic activities (Porter, 1992;
Crawford, 1996; Kirkwood and Best, 1998). Since the fates of many free-
living species are influenced by human activities, humans have an ethical
responsibility to injured wildlife welfare in the same way as they have for the
welfare of companion, farm and laboratory animals (Kirkwood and Sainsbury,
1996).
Keeping wildlife in captivity even temporarily or for rehabilitation
purposes poses many challenges, among which are ethical questions
concerning animal welfare. Indeed, welfare issues related to many aspects of
the recovery process (captivity, translocation, pain, human contact) can
influence the success of individuals’ survival capacity once they have been
released back into their natural habitats (Fajardo et al., 2000; Molony et al.,
2006; Tolhurst et al., 2016). Thus, concerns for wildlife welfare in
rehabilitation centers must be considered through the lens of rehabilitation
success, that is, the individuals’ survival capacity after their release to the
wild.
To provide guidance to wildlife rehabilitators in the area of wildlife
medicine, some clinical practice guidelines have been published which deal
with welfare rehabilitation standards (Miller, 2000; RSPCA, 2010; Miller,
2012), pre-release health screening protocols (Woodford, 2000) as well as
quality indicators of the rehabilitation process (Molina-López et al., 2013).
Captivity is the major source of distress since the facilities used for
confinement are designed for the safety of both humans and animals and
generally provide a barren and impoverished environment which generally do
not meet the natural needs of free-living wild animals (Mason, 2007; Morgan
and Tromborg, 2007).
The initial confinement, which is essential for injured wild animals when
they arrive at a rehabilitation center, is particularly stressful. The lack of
sensory stimuli that are essential for natural behavior, the reduced space to
limit movement and forced contact with humans are the major stress factors.
Several issues of wild animals’ welfare in rehabilitation centers are

common with other situations of captivity (e.g., zoos). For instance, basic
needs such as the provision of water and food follow the same requirements,
and the presentation, quantity and nutritional balance vary with the species,
size, and physiological and health status.
The provision of clinical care is the main activity of the rehabilitation
centers and it includes routine observations and records of each patient’s
condition, health and behavior, monitoring of the recovery process as well as
control of diseases and parasites.
The provision of a suitable environment depends on the species and is
determined according to the medical status of the patient and the requirements
of the recovery process. Hence, housing and caging are based on
approximations of space requirements during three recovery periods, each
defined by the activity level required of the patient (restricted
activity/mobility, limited activity/mobility, and unlimited activity/mobility).
Then, as the animal progresses through the rehabilitation process, indoor
caging is replaced by outdoor installations. Outdoor facilities (unlimited
activity/mobility level) generally use large and complex outdoor caging. These
enclosures must provide appropriate conditions to allow physical and
psychological conditioning or reconditioning of the patient by improving their
strength, developing stamina and coordination, restoring muscle tone, and
acclimatizing them to ambient weather conditions (Miller, 2012).
This last step of the recovery process provides appropriate conditions to
meet the physical and psychological needs of each individual, which fosters
the recovery of natural behavior. By re-creating as many of the positive
aspects of an animal’s natural environment and life as possible, environmental
enrichment is one of the most widely used and popular methods of improving
the welfare of wild animals in rehabilitation centers, promoting the frequency
and diversity of positive natural behaviors and increasing the animal’s ability
to cope with the challenges of the wild (Young, 2003; Mason et al., 2007). In
order to increase rehabilitated animals’ chance of survivability after their
release into the wild, environmental enrichment also reproduces some of the
negative features of the natural habitat that may reduce the welfare of these
animals (e.g., exposure to climatic conditions, parasites, etc.).
To be able to survive when they are reintroduced into the wild,
rehabilitated wild animals need to recover a wide range of skills such as the
ability to orientate and navigate around their environment, the capacity to feed
(hunting or foraging) and locate a safe place to rest, and the capability to
develop appropriate inter- and intra-specific interactions. Guidelines and
standards have been produced to enable the evaluation of the capacity of

rehabilitated wild animals to return to the wild (Soorae and Seddon, 1998;
Miller, 2000). As stated by the IUCN guidelines for the reintroduction of
rehabilitated wild animals, “the welfare of animals for release should be of
paramount concern through all stages.”
4. VETERINARY VIEWPOINT AND LIVESTOCK

The veterinary profession is privileged to occupy a position of enormous
social influence on animal welfare issues. However, the profession has
traditionally understood welfare primarily within the limited scope of animal
health and productivity. Currently, animal welfare focuses on companion and
farm animals, and welfare during transport of the animals and at slaughter.
However, there is no easy way to define the degree of freedom that an animal
should have as many factors are involved in the protection and welfare of
animals and the final purpose of its confinement (Ludewig, 2008). The present
trend among consumers, especially in more developed countries, is to seek out
foods produced under good animal welfare conditions, thus promoting a
change in the way animals are confined for food purposes. At present the
controversy is to decide on what degree of confinement actually affects animal
welfare.
The veterinary profession has contributed by and large in these fields, both
for the protection and reproduction of endangered wildlife species and for the
protection and welfare of domestic animals for food purposes.
4.1. Animal Welfare during Production
From the production point of view, the veterinarian overseeing a

production unit or working as a government inspector can enforce the laws
regulating how the animals/birds should be housed, fed and treated. For that
matter, it is necessary at the outset to be certain that the regulations in
developing countries are within the framework of those that already prevail in
developed countries.
The European Union has special regulations for the protection of farm
animals. Since their introduction in 1986, certain alterations and improvements
have been implemented regularly and as needed, with the current trend being
for breeding and raising livestock under natural conditions. These regulations
are based principally on a housing system that ensures the natural behavior of
the animal species, on feeding systems and on the treatment of animals during
this period until the time of loading for slaughter. However, it can be assumed
that these regulations are not yet being enforced in many developing countries.
Poultry and pork are the cheapest and most consumed meats worldwide and
more so in developing countries with their emerging economies (Marquer et
al., 2015).
Under the present circumstances, in developing countries, these
productions systems still follow the traditional model of household enterprises
and therefore need to be improved, creating a hybrid between the traditional
and the industrial mode of production. Though the conditions for housing of
poultry and pigs have greatly improved in developed countries, there is still a
dearth of information on how to transfer this knowledge and adapt it to local
conditions in developing countries.
4.1.1. Poultry – Broiler Production

Selection of animals/birds for breeding is an important factor of animal
welfare as genetically improved, rapid-growing animals certainly do not thrive
under conditions in the developing world, show greater stress levels leading to
lesser feed intake, and are more prone to diseases and with loss in final
slaughter weight. Nevertheless, advances have been made in recent years in
the European Union to improve the welfare of chickens kept for meat
production (cf. Directive 2007/43/EC of the European Parliament establishing
minimum rules for the protection of chickens for meat production), with
further suggestions by different authors to further improve the density/stocking
rate, together with an updated EFSA report on the welfare of broilers (Jong et
al., 2012). In spite of high broiler meat production within the EU-27 (9.6
million tons in 2011 and 10.5 million tons in 2014) and the existence of intra-
EU trade, the four major importers of broiler meat – the Netherlands, the UK,
France and Germany – trade not only within the EU zone but also import a
large quantity from third countries such as Brazil and Thailand (European
Commission, 2016a). However, the UK, the Netherlands, Germany, France
and Hungary are also the largest exporters of broiler breeders and grandparent
stock to countries outside the EU (Hiemstra and Napel, 2013), which leads to
the question of whether animal welfare regulations in these countries are being
followed to a level comparable with that in the EU (review in (Horne and
Achterbosch, 2008)). This is an important aspect as EU producers pay a high
price to maintain high welfare standards in all sectors of food production, and
standards may not be the same in developing countries, therefore leading to a
disparity in import pricing of meat products (Horne and Bondt, 2013). A

recent report on the effect of genetics on broiler welfare by the European
Commission to the European Parliament and the Council published in Brussels
on 7 April 2016 has stressed the fact that welfare problems could exist owing
to genetic factors mainly because the environmental conditions in breeder
selection farms are not the same as those in commercial farms and the fast
growth of the birds is not accompanied by ideal bone growth and
cardiovascular structures, leading to different types of injuries and cardiac
failure. The EU broiler breeders marketing genetically improved birds
currently offer two varieties: the fast-growing type and the slow-growing type.
These breeders have concentrated more on the selection of birds with
economic benefits rather than selecting for welfare traits. The current pressure
is on greater feed conversion rate, as feed costs are high and can represent up
to 65% of the production costs. Though no exact figures are available, it is
estimated that the slow-growing broilers make up only 5-10% of the total
broiler production and are used in organic and certified slow broiler farms
(European Commission, 2016a). However, in the developing world, these
slow-growing birds could be better as a parent stock than the rapid-growing
variety from the welfare point of view and could be crossed with local breeds
to maintain biodiversity.
4.1.2. Pig Production

Similar welfare problems also exist for pig production units in different
countries. In the EU, great changes were made to improve the welfare of pigs
bred in under intensive systems in compliance with the Council Directive
2008/120/EC to assure the comfort of the animals and their treatment. All EU
members had to comply with the group housing of sows and gilts except for
during short periods after service and at farrowing (European Commission,
2008). Recently, further recommendations have been made by the EU to
reduce the need for tail docking of piglets (European Commission, 2016b).
Advances have also been made to adapt different types of farrowing pens that
are more comfortable and give more freedom to lactating sows. By 1 January
2018 the castration of piglets will also be banned and searches for alternative
non-surgical methods are still going on.
The question is whether or not such welfare regulations and
recommendations are also being implemented in developing countries and
what is the current status of animal welfare is in general in the different
developing countries. This is an important issue to work on, and collaborations
between the EU and developing countries to work out the best methods to
solve possible problems could add many more milestones to the road for
improving the welfare of food producing animals. Faster-growing pigs with
greater final slaughter weight are the goals of many producers in the
developing world. However, in spite of the quest to improve food security and
profits in the developing world through the use of improved breeds of animals,
it is important to maintain the local animal germplasm that are more resistant
and better adapted to the local conditions (Godfray et al., 2010).
Crossbred animals could lead to better animal welfare owing to higher
resistance to diseases and stress under local circumstances. Further, avoiding
diseases in animals is very important for both human health and animal health
as many of the emerging diseases that occur today worldwide have their
origins in animals (FAO, 2013). Therefore, a better solution for developing
countries would certainly be sustainable production systems that support good
animal welfare and breeding animals from a strong genetic pool, with lower
animal density, better feeding facilities, regular veterinary inspections and a
lower incidence of diseases, the last being an important factor to avoid the use
of antibiotics, which we know is a major issue in today’s developed world.
A recent report by an international finance corporation (Mousseau et al.,
2014) on improving animal welfare in livestock operations gives extensive
information and guidance to improve animal welfare conditions in different
countries. Pig genetics have taken a similar path to that of broilers, thus
leading to the loss of biodiversity and a reduction in the number and variety of
local breeds in the world. A recent publication (Costa et al., 2015) has shown
the superior quality of meat of the local Portuguese piglet when compared with
exotic crossbred piglets, emphasizing the need to maintain local breeds - be it
in Europe or in developing countries. The breeding of pigs in intensive
systems to meet the great demand for meat supply has led to the abandonment
of rural farms and rural life with damaging consequences for biodiversity,
animal welfare and wildlife. However, many young European farmers today
are reverting to improved rural pig farming, following either the sustainable or
organic type of production with a better perception of animal welfare.
4.2. Animal Welfare during Transport and Slaughter
Within the European Union, animals are transported from the production
units to the slaughter house in accordance with EU regulation 1/2005 which,
for the protection of the welfare of the animals, defines the appropriate vehicle
for animal transport and the existence of trained personnel to carry out this
function. In non-EU countries where animals are exported to or bred, it is not

only animal welfare in the production units that can pose problems: there also
exists the question of the welfare of animals at the time of transport to
slaughter houses and the method of slaughter used in those countries. As
mentioned earlier, the fast-growing genetic variety that is used in commercial
farms is generally heavier and bigger.
This could lead to inadequate transport structures being available that
jeopardise the welfare of the animals during loading and transport. The
infrastructures available in different countries, such as the type of vehicle and
the type of cage used for birds (the genetically improved birds are bigger and
so need cages with larger openings), as well as the adequacy of vehicles, the
availability of loading ramps and their inclination in the case of pigs, animal
density, protection against heat, cold and rain, journey time, the type of road
and the distance to the slaughter house are some of the factors that should be
considered for global animal welfare. In many countries the animals have to be
transported over long distances in vehicles that are inadequate for the purpose
and over very bad roads before they reach the slaughter house. These slaughter
houses do not have the facilities to house these animals overnight to recover
from the journey nor the facilities to adequately stun the animals before
slaughter as required in the EU (European Commission, 2009), causing
extreme suffering to these unfortunate animals.
It is reported that the facilities available in many developing countries are
in appalling conditions, leading to abusive animal welfare at slaughter, a lack
of ante and post mortem inspections, unhygienic meat processing and
environmental pollution that is caused by poor sanitary facilities, all this
leading to public health hazards not only for the local population but also for
tourists that visit these countries (NKPAAA, 2009).
The veterinary health services in these countries, be they government
bodies or private firms, are responsible for implementing and maintaining
good animal welfare practices in different aspects of the food chain and also
guaranteeing good sanitary and environmental conditions. This requires the
participation of the society as a whole to ensure the adoption of the
recommended practices and would involve public awareness in the first place,
with sanctions or fines for those who do not abide by the rules.
5. CONSIDERATION
The subject of animal welfare was discussed from the viewpoints of
cruelty (ethics), wildlife conservation (environment) and veterinary attention
(science).
The majority of people believe that animals are currently raised without
cruel treatment, but reports of animal cruelty are not unknown – bear farming
typically entails the imprisonment of bears in squeeze cages for years (section
2). Habitat loss, climate change, poaching, and pollution paint a bleak picture
for threatened and endangered species around the world (section 3), and it is
estimated that at least about 10,000 species become extinct every year (WWF,
2016). The present trend among consumers, especially in developed countries,
is to seek out foods produced under good animal welfare conditions, thus
promoting a change in the way animals are confined for food purposes. At
present the controversy is to decide on what degree of confinement actually
affects animal welfare (section 4). It seems better to consider each issue
separately.
5.1. Abolition of Cruelty for Ethical Welfare
The majority of Westerners support the view that pain and suffering
should be minimised (Herzog et al., 2001). As stated in section 2, bears held
captive for bile extraction are kept immobile by crush cages on farms, and
catheters are inserted daily into the bears’ abdomens to drain their bile. The
bears moan in pain whenever the bile is extracted. When the bears cannot
produce sufficient bile, they are killed for their paws and gall bladders or are
left to die of starvation. Thus, it is only natural to conclude that all processes
on bear farms for bile extraction should be criticised based on the above-
mentioned concerns about animal welfare. However, bear farming for bile
extraction is legal in China.
5.1.1. Standardization
There is a great gap between Chinese legislation and cosmopolitan
concerns about animal welfare. The chief sources of traditional thinking about
animals’ status have been religion and philosophy, both of which have
interacted with science in shaping conceptions of what sorts of beings animals
are (DeGrazia, 2002).
To overcome this problem, it is essential to conceive international

standards that establish minimum agreed practices for the welfare of captive
animal species (pets and farm animals) at least, and it should be urgently
attempted to define what is considered an acceptable level of animal welfare
from the physiological and ethological viewpoints. It is expected that an
international agreement on animal welfare standards could serve to resolve
conflicts associated with ethical and cultural criteria. It is also advisable for
consumers to be informed about the welfare standards of animal products that
they are offered. Since Westerners seem to have a higher concern for animal
welfare today than they did 50 or even 25 years ago (AWWG, 2006), it can be
considered that today there is a strong possibility of internationally
standardising animal welfare.
5.1.2. Important Role of NGOs

Globalisation during the twentieth century gave rise to the importance of
non-governmental organizations (NGOs), so these organizations have
developed to emphasise humanitarian issues, developmental aid, and
sustainable development (Fisher, 1998). NGOs have also played significant
roles in the practical realization of animal welfare: for example, arousing
public awareness, sharing survey information, and raising the profile of this
issue during communications with national authorities and international
bodies.
Major sources of NGO funding include membership dues, grants and
private donations (Viravaidya and Hayssen, 2001). It is financially quite
difficult to promote animal welfare under the current system of NGO funding.
When the costs of an NGO’s core activities exceed the inflow of grants and
donations, it is forced to qualitatively and/or quantitatively reduce its work, or
to find new sources of funds to cover the difference. Reaching out to new
donors with innovative fund-raising approaches is usually the first step
(Viravaidya and Hayssen, 2001). An alternative funding approach is
essentially required with a view to enabling the promotion and realization of
animal welfare on a global scale.
5.2. Anthropogenic Impact on Free-Living Wild Animals
The anthropogenic impact on free-living wild animals’ welfare caused by

encroachment is a complex issue that involves a wide range of aspects and
stakeholders. Consequently, potential solutions that would prevent or minimise

such incidents should be developed in line with a broad and holistic approach.
Public authorities and non-governmental organisations must work together
with local communities that are under pressure owing to the proximity of wild
animals with a view to implementing sustainable alternatives. For instance,
public awareness, financial compensation for damage caused by wild animals
to crops and livestock, and the creation of protection buffer zones in order to
minimise direct contact between humans and wildlife are some of the many
ways that have actually been explored with the aim of increasing tolerance
among local communities toward the close proximity of wild animals and of
minimising human impact on wildlife welfare. In parallel, more efforts should
be made to develop and implement more humane programmes of wildlife
management (e.g., more humane culling methods, friendlier methods of
capture, transport or sterilisation, better selection of individuals to be relocated
in view of avoiding social separation, and better selection of a new
territory/habitat for relocation).
Some of the main issues regarding human impacts on the welfare of free-
living wild animals and potential solutions to minimise these effects were
recently addressed: wildlife welfare related to agricultural systems (Mathews,
2010), pest control programmes (Littin, 2012; Warburton et al., 2012) and
predation by domestic animals (Calver et al., 2007, 2011).
The welfare of wild animals as free-living or short-term residents in a
rehabilitation center is a quite recent concern and, although recent advances
have contributed considerably to an increase in knowledge in this field, further
progress is necessary to support the development of sustainable solutions to
minimise human impact on the welfare of free-living animals as well as to
increase the success rates of the rehabilitation process and the survivability of
released animals
5.3. Livestock
Apart from the boom in the human population, today’s society is also
becoming increasingly affluent, especially in developing countries, leading to
greater meat consumption even in countries that have not had a tradition of
high meat consumption and have depended on other protein sources to
supplement dietary needs.
According to a report by the Food and Agriculture Organization (FAO,
2011), meat consumption is projected to increase by 73% and consequently
global animal production is expected to almost double by the year 2050 in

developing countries whilst productions levels in the developed world remain
static. Awareness of animal welfare in developing countries is still very
rudimentary and veterinarians can play an important role in maximizing
awareness and implementation of animal welfare during production and
slaughter for food purposes.
Recently it was shown that live animals imported into an Asiatic country
for slaughter for local consumption were inhumanely processed, leading to
high stress levels for the animals (ABC, 2016). The increase in demand for
meat and the inadequate conditions presently available in developing countries
for the slaughter of animals will lead to more frequent incidents of violation of
animal welfare standards set in more developed countries.
Furthermore, the projected rise in meat consumption by 2050 means that
much of the future demand for livestock will be met by large-scale/intensive
operations, which could lead to a greater negative impact on animal welfare
and the environment, the effects of which can be attenuated only through
proper farm planning and appropriate training of personnel. For example, there
have been recent news reports of an increase in investment in pig production
in intensive systems by a Canadian company in India to meet the protein needs
of the increasingly affluent population of the zone.
This intensification of the pig industry should be sustainable so that the
rise in demand for meat protein is in keeping with the age-old tradition of a
balanced protein diet from different sources which is beneficial to human
health while including essential proteins from animal sources. However, the
intensification of pig production highlights two questions: what level of
welfare will be afforded to pigs in intensive farms considering that until now
the system of pig production in developing countries has typically consisted of
small rural farms? And secondly, what level of welfare will be provided for
animals at slaughter given that there are very few authorized slaughter houses
in these countries and most are probably located in major cities?.
Coordination at government level will be required for ensuring the welfare
of the animals and the quality of the product throughout the food chain. When
large scale or intensive production systems that are not very common in
developing countries are introduced, it is pertinent that the authorities in these
countries implement a sustainable method of production, which is a trend
currently gaining traction in European countries. The major question is: What
role does a veterinarian play in assuring the welfare of the animals? The
answers vary from genetics to management processes including the control of
diseases at the farm level.
CONCLUSION
Urbanization, the influence of the media and civil society organizations,
and higher levels of education are reasons for an increased interest in animal
welfare. Consideration of animal welfare should encompass not only the
physical health but also the psychological well-being of animals. The
importance of animal welfare differs from country to country owing to
differences in religion, economic development, education and perception.
Based on this complexity, animal welfare was discussed from different
viewpoints ‒ legal cruelty (bile extraction from living bears), Environmental
aspects (human impacts on free-living wild animals and wildlife rehabilitation)
and veterinary viewpoint (wildlife and livestock). The subject of animal
welfare is not restricted to the interests of a single field but interests both
scientists and the public. Although it is not enough to discuss only one aspect
of animal welfare, it may be concluded that an integrative approach is
necessary to describe the concept of animal welfare.
ACKNOWLEDGMENTS
Animal welfare is a significant topic even within the realm of harmonious
coexistence between humans and animals, but we have experienced the
dilemma between ideal animal welfare and the present situation through our
educational activities in zoology and volunteer activities in animal protection
and rescue (NANL in Japan and CERVAS in Portugal). It seems that the
majority of people believe that animals are currently raised without cruel
treatment, and there is a possibility that people may mistake the affectionate
treatment of animals as the standard that governs the broader scope of animal
welfare. We present this chapter in order to encourage a worldwide exchange
of views. The authors are grateful to Ms. C. Lentfer for English review.
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Chapter 3
BESTIALITY AND THE LAW: A FORM OF

ANIMAL PROTECTION OR PROTECTION OF
PUBLIC MORALS? A NEED FOR
REFORM-ANIMALS AS VICTIMS
OF SEXUAL ABUSE
Laura Donnellan *
School of Law, University of Limerick, Limerick, Ireland
ABSTRACT
Bestiality is a topic that evokes much revulsion and disdain. In
jurisdictions where bestiality is a criminal offence, the legislation has as
its focus the protection of public morals. It is seen as an abasement of the
person. At common law, the offence was enveloped in religious terms,
words such as “unnatural” and “abominable” were used to highlight the
perceived immoral nature of the crime. Bestiality was juxtaposed with
sodomy; both were viewed as moral equivalents that had no place in
polite society. Those that engaged in either act faced execution. Over
time societal attitudes towards homosexuality changed, however,
bestiality remains a heinous offence. The criminalisation of bestiality has
nothing to do with animal welfare. The fate of the animal is of little
concern to the legislature. The laws are drafted from anthropocentric
*
Corresponding Author: laura.donnellan@ul.ie.
88 Laura Donnellan
context; the offender in some ways becomes the victim as they are often
viewed as psychologically unwell and in need of treatment. Bestiality is
also viewed as a gate way crime, one that leads offenders to sexually
abuse children and vulnerable adults. Animals are used for many
purposes from food to clothing to entertainment and thus not seen as
having an existence outside the needs of humans. Humans have dominion
over animals and so long as the animal does not suffer unnecessarily, the
law does not intrude. While legislation may purport to protect animals
from unnecessary harm and suffering, the proprietary status of animals
permits harm so long as it is not gratuitous and constitutes good reason.
Why should bestiality be singled out? This chapter will examine the
justifications for the criminalisation of bestiality and will argue that
bestiality should be placed within the confines of animal welfare
legislation and the focus should be on the animal and respecting the
need to be protected from sexual abuse.
INTRODUCTION
The terms zoophilia or bestiality are often used interchangeably to denote
sexual relations between humans and animals. Zoophilia encompasses an
emotional element as well as a physical attraction on the part of the zoophile.
Whereas with bestiality, the bestialist is concerned with satisfying a sexual
urge. Sexual contact between humans and animals includes a broad spectrum
of activities including penetrative sexual relations, masturbation, frotteurism,1
exhibitionism, voyeurism,2 anal and oral sex.3 At common law the offence was
seen as a crime against nature and was punishable by life in prison. In Ireland
the Offences Against the Person Act 1861 juxtaposed sodomy and bestiality.
Only three of the twenty eight European Union member states, Hungary,
Finland and Romania, permit sexual relations with animals. The law in
Denmark was changed in July 2015. Prior to the amendment to the Animal
Welfare Act, sexual contact with an animal was only a crime if the animal
suffered harm. The reasons behind the amendment were twofold. It was
introduced partly to prevent animal sex tourism as there was anecdotal
evidence of animal brothels, clubs and organised animal sex shows. Denmark
1
Frotteurism in this context involves the rubbing of one’s genitals on the fur of a live animal, see
Aggrawal (2011), at 76.
2
Voyeurism and exhibitionism are defined by Aggrawal (at 74) as involving fantasies of
engaging in sexual relations with an animal or masturbating in the presence of an animal.
3
Penetration can be vaginal, rectal and by use of an object, Merck & Miller, at p.233.
Bestiality and the Law 89
had become a haven for zoophiles/bestialists as neighbouring countries,

Sweden, Norway and Germany, had all banned sexual intercourse with
animals. The other reason behind the ban was due to concern for animal
welfare.
The chapter will begin with a discussion of the terminology used and it
will then proceed to examine the reasons behind the criminalisation of
bestiality by drawing on the main arguments used: the harm principle, the
offence principle, animal cruelty, consent, morality and legal paternalism.
Each of the justifications will be challenged in order to ascertain which
provides the most solid base for the criminalisation of bestiality and the
corresponding intrusion by the state into the liberty of its citizens.
The chapter will then examine the law relating to bestiality in a number of
Member States in the European Union including Denmark, Ireland, England
and Wales. While laws around the European Union have been updated in
relation to bestiality, the offence of bestiality in Ireland is governed by the
Offences Against the Person Act 1861. In England and Wales the provisions
relating to bestiality fall under the Sex Offences Act 2003.
The chapter will conclude that bestiality/zoophilia should be referred to as
animal sexual abuse and by referring to it as bestiality or zoophilia the law
sanitises the offence. The law relating to animal sexual abuse is drafted from
an anthropomorphic view, with the focus being on the effect that bestiality has
on society as opposed to the effect it can have on an animal. The chapter will
contend that reclassifying it as animal sexual abuse would put the focus back
on the welfare of animals and not about regulating human morals. By placing
bestiality within the confines of animal welfare legislation, the argument in
relation to consent being irrelevant (as animals are used by humans for other
purposes, among them meat, clothing, hunting etc. and arguably do not
consent to such uses) can be removed from the discourse.
WHAT IS IN A NAME? ZOOPHILIA V BESTIALITY

While sometimes used interchangeably, there is a difference between the
two terms from the point of the human offender. Bestiality is the term used
when there is no emotional bond between the animal and the human, the
human engages in sexual relations with the animal in order to satisfy the
human’s sexual desires. A bestialist is opportunist in that s/he will have sexual
relations with an animal when there is no other “normal outlet for sex”
90 Laura Donnellan
(Aggrawal, 2008, at p.257).4 However, zoophilia refers to an emotional and

sexual attraction on the part of the zoophile. There are other terms including
zooerasty/zoorasty. A zooerast is similar to a bestialist; however, the zooerast
will have sexual contact with an animal even when normal outlets are
available (Aggrawal, 2008, at p.257).
Zoophilia is a medical term as it is classified as a paraphilia,5 which is
considered a mental disorder (Williams & Weinburg, at 524). 6 Crooks and
Baur (at p.536) categorise zoophilia as a form of coercive (and invasive)
paraphilia as the victim, the animal, is it is generally accepted is not
consenting to the sexual act. As will be discussed below, the issue of consent
presents a number of contextual difficulties.
From a legal perspective, the common term used is bestiality. Even within
the term bestiality, there are varying definitions depending on whether it is
defined from a legal standpoint or whether it is defined from the point of view
of religion (unnatural behaviour and non-procreative) or secular society
(deviation from accepted sexual norms, see Roberts, at 177 and 183). For
example, criminologist Piers Beirne (1997) defines bestiality as “interspecies
sexual assault” and contends that parallels can be drawn between animal abuse
and the abuse of women and children. Beirne adds that in almost all situations
of interspecies sex, the animal is under coercion, the animal may be harmed or
may suffer death as a result of the sexual encounter, the animal cannot consent
nor can the animal report the sexual abuse. Beirne (1999, at 139)
acknowledges the emotion and physical pain interspecies sex can have on an
animal.
Criminal lawyer Michael Roberts (at 180) offers a more clinical definition
and defines bestiality in the following terms: “Bestiality is sexual contact
between human and non-human animals for the purpose of human sexual
gratification.” Although Roberts (at 182) concedes that the definition fails if
the sexual contact between the human and animal is for money and not sexual
gratification. He provides the following example (at 182): a woman is paid by
another to have oral and vaginal sex with an animal while the other person
films the interaction. If the definition was applied in this situation, no offence
4
Merck & Miller at p.233 note depending on the size and type of animal, sexual relations may
result in the infliction of serious injury and lead to the death of the animal.
5
Paraphilia refers to sexual inclinations which transcend accepted norms. Norms change over
time, homosexuality being an example of what was considered deviant and a crime has now
been decriminalised in most Western societies.
6
The writers cite a newspaper article, Beastly passions (2000, December 3) The Independent on
Sunday, pp. 32–33 in which the author contends: “…Bestiality or zoophilia, as its apologists
prefer to call it…”
would be committed as no sexual gratification had occurred. It is simply a

business agreement. Arguably, most people would be repulsed by this and
would contend that irrespective of the sexual gratification of the human or lack
thereof, the animal is still the victim of “interspecies sexual assault.” Roberts
(at 182) extends the definition of sexual gratification to include “a purpose of
sexual gratification.” A purpose would include the resulting pornographic
material from the filming of the interaction as it could be argued that there is a
market for this and those who purchase the material are doing so for the
purposes of sexual gratification (Roberts, at 182). If the interaction is not
filmed and no sexual gratification is derived, then under Robert’s definition, it
does not constitute bestiality (Roberts, at 182-183).
In the recent Canadian Supreme Court case, R v D.L.W., the court clarified
the definition of bestiality to require penetration in order for it to be a crime.7
The case arose from the conviction of the accused of sexually abusing his two
stepdaughters over a ten-year period which included one count of bestiality.
He attempted to make the dog and one of his stepdaughters, who was a
teenager at the time, have sexual intercourse. When that did not happen, the
accused rubbed peanut butter on the girl’s genitals which the dog licked off
while the accused took photographs. He then requested that the girl do it again
so that he could film it. In the trial court, the judge held that penetration was
not required in order for an offence to be committed. It was accepted that the
accused derived sexual gratification from the sexual encounter between the
dog and the teenage girl. In applying Roberts’ terminology, the accused had
orchestrated the bestial act for his own sexual proposes. DWL appealed the
trial court decision to the Court of Appeal, with the majority quashing his
conviction on the grounds that the common law definition of bestiality
required penetration. Although Canada’s Criminal Code in 1955 placed all
crimes (with the exception of criminal contempt) on a statutory footing,
recourse to the common law is often made to augment the provisions of the
Code. The Offences Against the Person Act 1861 applied to Canada and was
transposed into the first English version of the 1892 Criminal Code. In 1955
the English version was amended and the offence of bestiality was expressly
provided for. The Code was revised in 1988 with the following section
referring to bestiality: Criminal Code, RSC 1985, c C-46. However, section
160 (1) does not define what constitutes bestiality. In the absence of a
definition and not willing to usurp the position of the legislature, the Court of
Appeal did not wish to depart from the accepted definition which requires
7
2016 SCC 22.
92 Laura Donnellan
penetration. If the definition was to be expanded to include oral sex, then that
would be a matter for Parliament. In a dissenting judgment in the Supreme
Court, Abella J argued that if bestiality and buggery where the same then there
would have been no need for the Code in 1955 to introduce a separate offence
of bestiality (at para. 144). Abella J referred to the case as one of statutory
interpretation (at para. 125). The majority upheld the Court of Appeal
decision. Thus, under Canadian law, in order for a crime to have been
committed penetration is required.
While Canada updated its bestiality laws in 1955, under Irish law, the
“unnatural offences” provisions of the Offences Against the Person Act 1861
still apply. Under sections 61-63, buggery and bestiality were referred to as
“unnatural offences” (which also would be the religious view of buggery and
bestiality). Homosexuality was decriminalised by virtue of section 2 of the
Criminal Law (Sexual Offences) Act 1993, however, the bestiality provisions
remain. Prior to the removal of buggery, section 61 prohibited buggery and
bestiality and provided a sentence of penal servitude for life or any term not
less than ten years. Section 62 provided that anyone attempting or intending to
commit either sodomy (or any indecent assault upon any male person) or
bestiality were guilty of a misdemeanour with the court being endowed with
the discretion to sentence the offender for up to ten years but not less than
three years of penal servitude or imprisonment for any term not exceeding two
years with or without hard labour. Section 63 defined carnal knowledge to
mean penetration only and ejaculation (“Emission of Seed”) was not needed to
prove that an offence had been committed.
As Ireland and England and Wales demonstrate, bestiality and sodomy
were juxtaposed as both were seen as crimes against nature. Sir William
Blackstone in his commentaries held bestiality and sodomy to be more heinous
crimes than rape. In relation to rape, Blackstone (at p.535) described it as “a
detestable crime” which “ought severely and impartially to be punished with
death.” In the next sentence, Blackstone is cautious and warns judges and
juries of falsehoods and malicious witnesses. Given the repulsion to such a
crime, judges and juries, Blackstone adds (at p.535), can too hastily convict
the alleged offender and be swayed by deceitful allegations. In relation to
bestiality and sodomy, Blackstone (at p.535) contends that it “is the more
detestable… of a still deeper malignity; the infamous crime against nature,
committed either with man or beast.” Blackstone proffers that sodomy and
bestiality are moral (and criminal) equivalents. As with rape, Blackstone (at
p.535) warns against false allegations:
“A crime which ought to be strictly and impartially proved, and then

as strictly and impartially punished. But it is an offence of so dark a
nature, so easily charged, and the negative so difficult to be proved, that
the accusation should be clearly made out: for, if false, it deserves a
punishment inferior only to that of the crime itself.”
With the terminology of bestiality and zoophilia aside, there is no concrete

or universally accepted legal definition of bestiality. As will be seen with the
discussion on Ireland, the judiciary has great discretion in relation to the
definition of buggery of an animal and have found an offence had been
committed in one case by the owner of a dog who had co-opted a woman to
have penetrative vaginal sex with his male dog. Thus in some jurisdictions,
such as Ireland, the courts have used artistic licence in order to expand the
definition from the legislation, while others, such as Canada, have adopted a
very narrow definition of bestiality.8 Legislating for morals presents a number
of theoretical difficulties and the immorality of bestiality may be contested by
those who contend that bestiality should not be a criminal offence, especially
in situations where the animal is unharmed. It is to the justifications for the
criminalisation of bestiality that the chapter now turns.
JUSTIFICATIONS FOR THE CRIMINALISATION

OF BESTIALITY
A number of arguments have been advanced as to why bestiality should be

prohibited. Each argument can be challenged by a countervailing argument.
The main justifications are as follows: the harm principle, the offence
principle, animal welfare, consent, legal paternalism and morality.
The Harm Principle
Depending on the sexual act, an animal can be harmed resulting in serious

injury or death. At the core of the harm principle is the balancing of individual
liberty or autonomy with order in society. Restrictive measures should only be
8
In R v D.W.L., 2016 SCC 22, the Canadian Supreme Court adopted a very narrow definition and
relied on the common law definition of penetration. Judge Moran in the Circuit Court case
discussed under Ireland extended buggery to include vaginal penetration.
94 Laura Donnellan
taken by the state in order to prevent the infliction of harm to others. John
Stuart Mill (at p.8) proffered: “The only purpose for which power can be
rightfully exercised over any member of a civilised community, against his
will, is to prevent harm to others.” However, “others” does not apply to
animals (Roberts, at 193). Animals are used by humans for food, sport,
clothing, entertainment and experimentation, among other uses. To prohibit
bestiality on the basis of the harm principle leads to inconsistency as it is not
applied to other animal uses. Roberts (at 195) suggests the extension of
victimhood to animals in order to satisfy the “others” requirement.9 However,
there are two main impediments to animals falling within the definition of
others: one being “empirical and the second problem theoretical” (Roberts, at
195).10 In legal systems where bestiality is considered a crime against nature,
the objective of the legislation “is to protect moral decency and not nature”
(Roberts, at 195-196). Statutes that classify buggery as crimes against nature
are usually accompanied by the words “detestable” and “abominable,” these
words have a moral meaning originating from the Bible (Roberts, at 196). The
intent of the legislature is not to prevent harm to others but is founded upon
the protection of moral decency (Roberts, at 196). Historically, bestiality was
prohibited on the ground of public morals (Jones, at 530). During the reign of
Henry VIII the first civil statute prohibiting sodomy in 1533 was enacted, with
the full title of “An Acte for the punishment of the vice of Buggerie.” 11
Previous to this, it had been within the domain of the ecclesiastical courts to
deal with cases involving homosexuality and bestiality. The Act defined
buggery as a “detestable and abominable vice…committed with mankind of
beast.” The penalty was death by hanging. One of the main reasons, outside of
morality, for introducing this Act was to dilute the power of the ecclesiastic
courts as Henry VIII had already seized Church property and viewed the
introduction of this Act as a further diminution of the Church’s power (H.
Montgomery Hyde, at p.40).
The intent of the legislature under existing bestiality legislation is to
protect human morals and, arguably, has nothing to do with animal welfare or
cruelty. In relation to contemporary animal welfare legislation, the provisions
are based around the animal not being subjected to unnecessary harm or
suffering. Under animal welfare legislation, harm is permitted so long as it is
necessary and there are no viable alternatives to the infliction of suffering on
9
See also Joel Feinberg, at pp58-59 for his discussion of animals and welfare interests.
10
Theoretical refers to consent.
11
25 Henry VIII (1533), c. 6. This Act was repealed by the Offences against the Person Act 1828
(9 Geo.4 c.31).
the animal. Unless there is a specific provision which prohibits bestiality

within the confines of animal welfare or anti-cruelty legislation, the harm
principle is difficult to argue as it will be countervailed by those that will base
their arguments on irrationality and inconsistency.
The roots of bestiality being perceived as immoral stem from the
dominion status of animals, a view very much espoused in traditional religious
teachings (Jones, at 530). Animals were traditionally viewed as inanimate
objects, pieces of personal property that could not be ascribed rights. Animals
were not considered to have an existence outside the needs of humans. An
example of the religious view of animals, Saint Thomas of Aquinas argued that
humans, as possessors of a soul, had dominion over animals to do whatever
they wished. Saint Thomas of Aquinas reinforced the view of the Christian
Church that animals were inferior to humans. Morriss (at 272) does not believe
that bestiality was prohibited because it was viewed as a “degradation of the
animal”; instead he posits that it was reviled as it confused “the boundaries
between the species.” He (at 272) aptly explains his proposition:
“My suggestion is that there is abhorrence, not because it degrades

animals, but because it upgrades them - it treats them as something better
than they are. Sexual intercourse is supposed to be a sign of love; it is
supposed to be carried out between creatures of approximately equal
standing. For a human to have sexual intercourse with an animal implies
that the animal is of equal standing to the human. It denies a hierarchy in
which animals are always lower than humans. So it blurs, or denies,
boundaries, particularly the boundary between the human and the
animal.”
The contention that bestiality is a gateway offence to other crimes is often

used to support the application of the harm principle to bestiality. 12 Beirne
(2001, at 52) refers to two main arguments in favour of criminalising bestiality
in the debates that surrounded the proposal to introduce legislation in Maine to
prohibit bestiality: “one that bestiality is a form of animal cruelty in and of
itself and that it is a form of violence linked to other forms of violence,
particularly in the family.”13 In regard to the argument that bestiality is linked
12
Pegg & Davis, at p.128 refer to bestiality as a “gateway offence, one that could lead to
offending against other vulnerable victims,” most notably children.
13
Only two people publically denounced the proposed legislation. One on the grounds that there
were not enough prisons in Maine and the second individual argued that bestiality was a form
of sexual orientation and that not only did he derive pleasure from sexual relations with his
dog, his dog also enjoyed it.
96 Laura Donnellan
to other forms of violence, Beetz (at 8) refers to a study carried out by

Grassberger in 1968 that found between 1923 and 1937, 750 men in Austria
were convicted of sexual contact with animals. Fifty one of the 750 cases were
reviewed in detail and Grassberger found that 87% had been convicted once of
bestiality and 13% had been convicted again for bestiality and or other sexual
crimes (Beetz, at 8). Grassberger concluded that bestiality was a very rare
offence and the typical offender is aged between 14 and 23 (Beetz, at 8). The
argument that bestiality is linked to other sexual crimes has been greatly
undermined and in many situations those that engage in bestial acts are often
considered to be mentally unwell and “has now become more and more an
issue for psychiatry” as opposed to the offender being considered a criminal
(Beetz, at 9).14 However, if that logic is applied to sexual contact involving a
child or a vulnerable adult, the offender would be subject to the full rigours of
the criminal law and while mental impairment may be a mitigating factor, it
would not absolve the offender from criminal sanction. In equating bestiality
with animals and sexual abuse of children and vulnerable adults is ascribing
legal personhood to animals. However, as animals are defined as property such
an ascription is not possible and it is doubtful it will ever be possible.
Studies in relation to bestiality as a gateway offence to other sexual
offences are contradictory. In a study carried out by Frazier in 1997, the link
between bestiality and other sexual offences was quite prevalent among
juvenile offenders with 37% of sexually violent juvenile offenders also being
found to engage in bestiality and sexual abuse of animals (Frazer as cited by
Ascione, at p.54). Ascione asserts that such findings may be construed as
animal sexual violence being a “form of rehearsal for human-directed
violence” (Ascione, at p.54). The problem with establishing concrete evidence
to support this hypothesis is the very private and secretive nature of bestiality.
Beirne refers to underreporting as offenders might be charged under public
indecency or animal cruelty legislation and not under bestiality.
Another important consideration in discussing the harm principle and its
application to bestiality is that of situations where the animal is not considered
to have suffered during or as a result of the sexual contact. In this situation it
would be very difficult to justify the criminalisation of bestiality. There are a
14
This view was also supported by Germany when it removed the prohibition on bestiality. It
was reintroduced again in 2012. The committee behind its removal in 1969 was of the opinion
that only those with a mental impairment or a juvenile would commit such an act and thus they
could not be held responsible for their actions, Beetz, at 6. See also Dennis J. Baker, at p. 83
submits that duelling would fit within the harm principle, however, bestiality “would not set
back the interests of others and therefore psychiatric and therapeutic treatment should be made
available to assist those who engage in this type of abnormal conduct.”
number of factors to consider including the size of the animal and whether it
has been involved in penetrative sex or oral sex. Harm is defined from the
human perspective. While lesions and other injuries are visible signs of harm
on an animal, it is very difficult to discern the mental harm, the distress caused
to the animal. The use of the criminal law can be a blunt instrument when it
comes to bestiality. Animal welfare or anti-cruelty statutes may provide more
concrete grounds for the prohibition of bestiality. Under the Animal Welfare
Act, 2006 (England and Wales), animal welfare is divided into two broad
groups-the promotion of animal welfare and the prevention of harm to
animals. The Act (section 9 (1)) creates a duty of care which is placed on the
person responsible for the animal. The person responsible for the animal must
ensure that the animal’s needs are met, to the extent required by good practice.
Within the rubric of the promotion of animal welfare, section 9 (2) provides
for five freedoms: its need for a suitable environment, its need for a suitable
diet, its need to be able to exhibit normal behaviour patterns, any need it has to
be housed with, or apart from, other animals, and its need to be protected from
pain, suffering, injury and disease.15 It is contended that bestiality could fall
within the freedom relating to the need to be able to exhibit normal behaviour
patterns. The freedom could be expanded to include the protection from sexual
abuse as arguably animals are not predisposed to be being sexually attracted to
humans. While there have been claims that dolphins have exhibited sexual
attraction to humans, most animals would, in exhibiting normal behavioural
patterns, not naturally engage in sexual relations with humans.
In relation to zoosadism where the human derives sexual pleasure from
inflicting pain and suffering on the animal, the harm principle can be clearly
justified. Zoosadists may use a large object to penetrate the animal and such
actions undoubtedly would cause pain and suffering (Beetz, at 7).
The Offence Principle
Bestiality is often justified on the grounds of public offence. This raises a

number of conceptual difficulties when it comes to bestiality. The principle of
public offence contends that the state is justified in legislating against
behaviour that evokes feelings of disgust that either results from an individual
directly observing the offending behaviour or indirectly from being informed
15
It could be argued that animals are exposed to disease when engaging in penetrative sex with a
human.
98 Laura Donnellan
of the disturbing event (Roberts, at 205). In order to satisfy the principle, there
must be a causal link between the mental unpleasantness and the actions of the
offender and there must be resentment on the part of the individual towards the
offender who has placed them in such a situation (Roberts, at 205). A number
of factors must be considered including the seriousness of the offence, the
duration, the assumption of risk of the offended person and also it must be
shown that the sensibilities of the person are not of such a level that it is a
disproportionate reaction (Roberts, at 205). There also has to be a balancing
act of the infringement of someone’s liberty, the sensibilities of the offended
individual and that of the state in incurring cost in enforcing the law (Roberts,
at 205). The offence principle is undermined by the fact that most bestial acts
take place in private and thus makes it difficult to prove that anyone was
offended. Bestiality would generally be considered to be socially unacceptable
and that justifies the intrusion of the legislature (McCutcheon, at 28).
Devlin, an advocate of legal moralism, contended that disgust was a
sufficient reason for the criminal law to regulate human behaviour. However,
when it comes to legislating for morals, there has to be an acknowledgment
that morals change over time and what is acceptable at one time may not be
acceptable at another time. Behaviour which is deemed to be immoral and
subject to the machinations of the criminal law results in certain behaviour
being penalised while other perceived immoral behaviour is immune from
state interference. Germany removed the prohibition on bestiality in 1969;
however, it was re-instated in 2012. In Ireland, homosexuality was
decriminalised (for persons over the age of 17, see sections 3 and 4 for the
provisions relating to those under the age of 17) under section 2 of the
Criminal Law (Sexual Offences) Act 1993. This Act repealed sections 61 and
62 of the Offences Against the Person Act 1861 (save in so far as they apply to
buggery or attempted buggery with animals). It was as a result of Ireland’s
obligation under the European Convention on Human Rights (ECHR) that the
state removed the prohibition on homosexuality. 16 Devlin (at p.17)
acknowledged that human sensibilities change over time; morals are in a
constant flux as the example of animal cruelty demonstrates:
16
See Norris v Ireland, Application no. 10581/83, Council of Europe: European Court of Human
Rights, 26 October 1988, available at: http://www.refworld.org/docid/48abd5a2d.html
accessed 19 August 2016. The European Court of Human Rights held that Ireland was in
breach of Article 8 of the Convention on the right to respect for private life which includes the
right to a sexual life.
“No society can do without intolerance, indignation, and disgust;

they are the forces behind the moral law, and indeed it can be argued that
if they or something like them are not present, the feelings of society
cannot be weighty enough to deprive the individual of freedom of choice.
I suppose that there is hardly anyone nowadays who would not be
disgusted by the thought of deliberate cruelty to animals. No one
proposes to relegate that or any other form of sadism to the realm of
private morality or to allow it to be practiced in public or in private. It
would be possible no doubt to point out that until a comparatively short
while ago nobody thought very much of cruelty to animals and also that
pity and kindliness and the unwillingness to inflict pain are virtues more
generally esteemed now than they have ever been in the past. But matters
of this sort are not determined by rational argument. Every moral
judgement, unless it claims a divine source, is simply a feeling that no
right-minded man could behave in any other way without admitting that
he was doing wrong. It is the power of a common sense and not the
power of reason that is behind the judgements of society.”
In applying the above arguments, those espousing liberal views will

contend that something cannot be deemed immoral simply because it offends a
person’s sensibilities. The offence principle, while an important consideration
in the argument in favour of the criminalisation of bestiality, may be
countervailed on the grounds that bestiality often takes place in private.
Animal Cruelty
A more solid basis for justifying bestiality laws is that of animal cruelty.
However, Peter Singer contends that interspecies sex is not always a form of
cruelty. In his opinion piece entitled Heavy Petting, Singer raises an
interesting argument:
“Who has not been at a social occasion disrupted by the household

dog gripping the legs of a visitor and vigorously rubbing its penis against
them? The host usually discourages such activities, but in private not
everyone objects to being used by her or his dog in this way, and
occasionally mutually satisfying activities may develop.”
In the above situation, the animal is not being harmed and has initiated
sexual contact with the person’s legs. However, in another example, Singer
100 Laura Donnellan
refers to the use of hens and contends that the cruelty involved justifies the
prohibition on bestiality:
“Some men use hens as a sexual object, inserting their penis into the
cloaca, an all-purpose channel for wastes and for the passage of the egg.
This is usually fatal to the hen, and in some cases she will be deliberately
decapitated just before ejaculation in order to intensify the convulsions of
its sphincter. This is cruelty, clear and simple.”
In the next sentence, Singer highlights the inconsistencies when it comes

to battery hens that are kept in captivity. Singer asks:
“But is it worse for the hen than living for a year or more crowded
with four or five other hens in barren wire cage so small that they can
never stretch their wings, and then being stuffed into crates to be taken to
the slaughterhouse, strung upside down on a conveyor belt and killed? If
not, then it is no worse than what egg producers do to their hens all the
time.”
When examined from the point of animal cruelty, animals are subjected to
abject cruelty in many situations, intensive factory farming as pointed out by
Singer, so why single out one particular aspect, in this situation bestiality?
Similar arguments can be traced back to the debates surrounding the
introduction of the Ill-Treatment of Cattle Act in 1822 (also referred to as
Martin’s Act as it was introduced by Richard Martin MP), the world’s first
contemporary animal welfare statute. 17 Prior to the 1822 Act, numerous
attempts were made to undermine the legitimacy of legislating for the
protection of animals. Each Bill presented would be rejected by the opposition
arguing that not all animals were protected and that it was a class issue as the
animals targeted were animals identified with the working class.18 In February
1824, Richard Martin attempted to extend the 1822 Act to include dogs, cats,
monkeys and other animals 19 and also introduced a Bill to prohibit Bull-
17
An Act to prevent the cruel and improper treatment of Cattle, 3 Geo IV, c71.
18
For example, Lord Erskine introduced: “An act to Prevent Malicious and Wanton Cruelty to
Animals” on the 5th of May 1809. The Bill made it illegal to beat a horse, donkey, ox, sheep
or pig. The notable exceptions were bears and bulls, neither of which was mentioned in the
Bill. Erskine admitted that the bill did not apply to the whole animal world as to do so would
subject the bill to “insurmountable difficulties, and the whole bill might be wrecked by an
impracticable effort to extend it,” Parliamentary Debates from the Year 1803 to the present
year, at pp.557-558.
19
Cattle Ill-Treatment Bill, The Parliamentary Debates, cc.865-69.
baiting and other cruel practices.20 In June of 1824, Martin introduced a Horse
Slaughtering Bill,21 while in February 1825; once again Martin endeavoured to
re-introduce a bill on bear-baiting, badger-baiting and dog fighting.22 In March
1825, Martin attempted to make offences under the 1822 Act misdemeanours
which would have resulted in a fine and imprisonment. In April 1826, Martin
sought to introduce a Bill to protect dogs; 23 Mr. Hume argued that cats should
be included,24 while Secretary Peel made a similar argument.25 Martin argued
that the comments were absurd. He asked did that logic mean if 500 people
were cast upon a rock in a desolate island and could not all be saved, that
would mean none of them could be saved. 26 Although Martin made an
impassioned appeal in his speeches, none of the Bills succeeded.
If it is accepted that the hen in the cage suffers as much pain if not more
than the hen who is sexually abused, does that mean that bestiality should be
permitted in order to ensure consistency? Martin’s response about 500 people
cast upon a rock is as relevant today as it was in 1826. Inconsistencies aside,
the prohibition on bestiality at least, in theory, protects animals from sexual
abuse.27 Throughout this chapter it has been noted that bestiality often takes
place in private, there is a lack of reporting and when it reported to the
authorities, individuals are sometimes prosecuted under public order or animal
cruelty legislation. While questions may be raised about the enforcement of
the law, the prohibition of bestiality on grounds of animal cruelty is
nevertheless important and main be viewed as a bastion of commitment to
social reform.
20
Bear Baiting Bill, Parliamentary Debates, at cc.131-34.
21
Parliamentary Debates (New Series Commencing with the Accession of King George IV), at
cc.1095-97.
22
Bear-Baiting Bill, Parliamentary Debates (New Series Commencing with the Accession of
King George IV), at cc.657-61. Mr. Gordon referred to the Bill as “petty legislation” (at
c.660), while Mr. Buxton (at c.660) referred to the success of the 1822 Act and its “beneficial
change in the manners of the lower orders, and was far from having produced that unnecessary
litigation which some gentleman had anticipated.” He noted that 69 convictions had been
secured under the Act. Mr. Butterworth (at c.661) asked if Mr. Martin would extend the Bill to
the “savage, abominable, and unchristian practice of prize-fighting, which had led in many
recent instances to the loss of life.” The Bill was defeated by 41 votes to 29.
23
Bill to prevent the cruel and improper treatment of dogs, at cc.530-2.
24
Ibid., c.530.
25
Ibid., cc.530-1. Mr. W. Smith (at c.531), while opposing the Bill, proffered that acts of cruelty
should be classified as misdemeanours. Martin withdrew the Bill with a view to introduce a
more comprehensive bill in the future.
26
Bill to Prohibit Bull-Baiting and Dog Fights, at cc.433-35, at c.433.
27
For a discussion on practicalities of enforcing legislation, see Roscoe Pound.
102 Laura Donnellan
Consent
Consent presents a number of theoretical difficulties. Zoophilia ascribes

an emotional and sexual bond between the zoophile and the animal. It is
evaluated from the perspective of the human offender. Whether there is
emotion or simply a desire to fulfil a sexual urge, is irrelevant to the animal
victim. The animal is not able to consent to sexual relations and may suffer
harm and possible fatal injuries due to the actions of the offender. Admittedly,
the issue of consent raises a number of contextual difficulties as animals do
not consent to being used for food or sport. Humans also have dominion over
the reproductive rights of animals.28 However, there is a difference between
rights and welfare. Proponents of animal welfare campaign for the
introduction of anti-cruelty legislation, those who work in humane societies
call for minimum standards to be introduced that require humane treatment of
animals. The term animal welfare is a broad concept that prohibits the
infliction of unnecessary pain, suffering or distress by humans to an animal
either in their care or an animal that has come in contact with them (Sankoff,
at p.7). Animal rights supporters, on the other hand, view animals as having
rights. As a rights holder, animals should “be treated as ends, not means”
(Sunstein & Nussbaum, at p.5). In invoking this Kantian idea, animals should
be afforded protections that go beyond prescribing minimum standards of care.
Animals should have the right not to be consumed or used for clothing
purposes, the right not to be hunted, the right not to be used in experiments,
the right not to have their liberty deprived in a zoo or a circus (Sunstein &
Nussbaum, at p.5). Advocates of animal welfare receive broader support, as
ascribing rights to animals is not widely accepted in contemporary society
(Sunstein & Nussbaum, at p.5). Such reluctance can be attributed to the fact
that not all humans have equal rights so to ascribe rights to beings that are
considered inferior to humans, for some it is an unsettling expansion of rights.
Taking property law as an example, property has proved to be a gendered
concept. For centuries property law has frowned upon women owing property.
It has continually reinforced and encouraged traditional gender roles and has
incorporated an “Anglocentric bias” (Thornton, at 491). Thornton (at 491)
notes: “others, whether they be women and/or Aboriginal people, are
perennially placed in the situation of having to contest rights to property and
28
Haynes (at 132-133) highlights the inconsistencies. He refers to the fact that companion
animals are spayed or neutered, livestock animals are often castrated by farmers and
artificially inseminated. No regard is given to consent in these situations.
citizenship.” 29 Property law envisages an ideal landowner: “white, middle-

class and male” (Dorsett, at p.279). Those who fail to emulate the ideal are
seen as unworthy property owners.
In returning to the issue at hand, consent or lack thereof and bestiality
present a theoretical conundrum. However, by placing bestiality within the
confines of animal welfare, it is accepted that animals can suffer and that us as
humans are obliged to ensure that animal suffering is minimised. Arguably,
animal welfare incorporates an element of rights. At the core of both sides of
the argument, is the right of an animal to be protected from suffering (Sunstein
& Nussbaum).
The Legal Regulation of Morals
The criminalisation of bestiality in Denmark did not receive the support of

the Danish Animal Ethics Council who viewed the new law as a form of
regulation of human morals. The Danish Ethical Council for Animals was of
the opinion that existing animal welfare laws already protected animals from
unnecessary suffering and that the amendment was superfluous. The Council
Chairman, Bengt Holst in espousing the anthropomorphic view, referred to the
control humans exert over animals when it comes to reproductive rights:
“It is us humans who control when and how an animal is allowed to

reproduce. When one draws the semen of a stallion for artificial
insemination, you are doing exactly the same thing as if you were having
29
This contention can be seen in the way the purchase money resulting trust under
Irish law requires an express agreement between the parties when it comes to
indirect contributions to the purchase price of the property. The non-legal
owning spouse or partner (traditionally the woman) will have to prove that
there was an express agreement in order to gain a beneficial interest. In recent
years, the introduction of legislation, Civil Partnership and Certain Rights and
Obligations of Cohabitants Act 2010 as amended, for those in registered
partnerships (same couples) and cohabitees (of either sex or same sex
couples) means that couples have other avenues of redress. However, in
situations involving those that do not wish to go the formal separation or
divorce route or there is a judgment mortgage involved and the parties are not
dissolving their relationship, the equitable device of the purchase money
resulting trust is still used.
104 Laura Donnellan
sex with an animal. Physically, it is the same thing you do with the
animal.” 30
Scientists also entered the debate with one proffering that the size of the
animal is an important consideration. While penetrative sex would harm a hen,
a cow or horse would arguably not be hurt (Christiansen). Dr Christiansen
further argued that there was no evidence to suggest animals did not enjoy
interspecies sex and that animals often enjoy sex for pleasure and not for the
purposes of reproduction. However, Dr Christiansen did not refer to any
literature where interspecies sex was reported to be enjoyed by animals.
As the discussion on the harm principle demonstrated, the intrusion of the
state into the liberty of individuals can only be justified if there is harm and in
balancing the interests of individual autonomy and protecting others from
harm. By definition, “others” excluded animals. In general, most moral based
legal provisions are uncontested. Where tension does arise is in situations
when the moral underpinning of the law is not “protecting others from fairly
direct harms” (Greenawalt, at 710). Greenawalt (at 723) cites two examples,
bestiality and bear fighting, and states that “these examples show that even in
liberal democracies, a sense of objective immorality affects feelings about
legislation.” The motivation behind these has nothing to do with animal
protection. Sexual intercourse with a different species can cause the transfer of
diseases or illnesses to the human. Animal fighting sports are often banned due
to the fear of the effect it will have on inter-human relationships with regard to
violence and aggression (Greenawalt, at 723). The prevailing attitude that such
activities are immoral and lead to the abasement of the individual is also a
consideration. However, in a liberal society the regulation of morals and
personal autonomy are difficult to reconcile.
Legal Paternalism
Legal paternalism is cited as one of the justifications in support of the

criminalisation of bestiality. The law assumes a parental role over society in
order to save some individuals from themselves. However, there are very few
reports of bestiality in Ireland, for example. If it is accepted that bestiality
rarely occurs then the chances of someone being harmed is negligible, this
undermines the state’s intrusion into the liberty of its citizens. Legal
30
The Local. Bestiality ban not needed: Ethics Council.
paternalism in contrast to the harm principle is concerned with protecting the

person themselves from self-harm and not from harming others. Both Roberts
and Baker discuss self-harm with Baker (at p.83) applying it to incest drawing
from his discussion on bestiality. Baker contends that the appropriate action is
psychiatric and therapeutic treatment. For him bestiality does not involve the
setting back the interests of others, similarly, with incest between two
consenting adults, “paternalism does not provide a sound basis for
criminalisation let alone a justification for sending people to prison” (at p.83).
Within the context of legal paternalism, the protection of public health is
also used as a justification for the prohibition of bestiality. If it is accepted that
bestiality is very rare then the chances of disease spreading is insignificant
(Roberts, at 204). Owners of animals are very unlikely to engage in sexual
relations with an animal that is known to them to be ill. If the human in
question is not the owner then s/he has infringed the property rights of the
owner.
ANIMALS AS PROPERTY: ANOTHER CONSIDERATION

Ireland, as a common law jurisdiction, defines domesticated animals as
personal property. While legislation may purport to protect animals from
unnecessary harm and suffering, the proprietary status of animals permits
harm so long as it is not gratuitous and constitutes “good reason” (White, at
p.79). Arguably, bestiality would not constitute “good reason.” In most
common law jurisdictions, it is a criminal offence to intentionally inflict pain
or suffering on an animal. The term animal welfare is a broad concept that
prohibits the infliction of unnecessary pain, suffering or distress by humans to
an animal either in their care or an animal that has come in contact with them
(Sankoff, at p.7). If there is no harm caused to the animal, then no criminal
offence has been committed.
There are, however, limits to the proprietary interest of the owner when it
comes to the unreasonable and unnecessary infliction of harm. Animal welfare
laws do not grant rights to animals. The legal system grants rights to humans
in general and in the situation of animals, the human is protected more
specifically by property laws. Animal welfare legislation restricts the use of
animals in much the same way as restrictions are placed on the use of property
(Francione, at p.4). Animal welfare legislation balances the interests of
animals against the interests of humans. In most situations, the balance tips in
favour of the human. Anti-cruelty laws or laws governing the use of animals
106 Laura Donnellan
primarily require that animals are not subjected to unnecessary or inhumane

treatment. Little or no direct duties are placed on humans. Humans are not
required to consider the welfare of the animal itself. Legislation may prohibit,
for example, animal testing on cosmetics or the trade in the fur of companion
animals, however, the welfare of the animal is a secondary consideration. The
legislation is often in response to consumer preference and market forces
(Donnellan).
With the justifications and terminology providing a contextual
background, the next part of the chapter examines the law relating to bestiality
in Denmark, England and Wales and Ireland.
THE LAW RELATING TO BESTIALITY IN DENMARK

Denmark enacted legislation in 2015 which makes it an offence to have
sexual intercourse with an animal. While sexual intercourse with animals had
previously been criminalised in Denmark, it was only a crime if there was
unnecessary suffering on the part of the animal. Denmark included the offence
within its Animal Welfare legislation. There were two reasons behind the
amended legislation. There were reports of animal brothels and sex shows in
Denmark as Germany had banned bestiality in 2012, resulting in an increase in
animal sex tourism in Denmark. Even before the ban in Germany, there was
evidence of animal sex shows in Denmark. This was backed up by a UK
Select Committee on Culture, Media and Sport Minutes of Evidence in
relation to a Memorandum submitted by the Internet Watch Foundation (IWF)
from January 2008.31 The IWF stated: “A search on the internet using the word
‘bestiality’ and with filters turned off returns thousands of hits; the top one is a
website of humans engaged in sex acts with animals which is hosted in
Denmark.” Denmark had become a haven for zoophiles as neighbouring
countries, Sweden, Norway and Germany, had all banned sexual intercourse
with animals. Under German law, which was introduced in 2012, an individual
found to have engaged in sexual intercourse with an animal faces a fine of up
to €25,000.32 The other reason behind the ban was due to concern for animal
welfare as the Minister for Food, Agriculture and Fisheries, Dan Jørgensen, an
31
See: http://www.publications.parliament.uk/pa/cm200708/cmselect/cmcumeds/353/8022609.
htm.
32
RT News, Animal urges: Bestiality ban passes Bundestag.
advocate of animal welfare, was quoted as stating: “the most important is that
in the vast majority of cases it’s an attack against the animals” (Christiansen).
While sexual intercourse with animals had previously been criminalised in
Denmark, it was only a crime if there was unnecessary suffering on the part of
the animal. Minister Jørgensen contended that it was difficult to prove that the
human had caused unnecessary suffering and that the benefit of doubt had to
be given to the animal as “an animal by its very nature cannot say no.”33 The
amended 2015 Act explicitly makes it an offence to have penetrative sex with
an animal and is punishable by one-year imprisonment for a first infraction
and two years for repeat offences.
THE LAW RELATING TO BESTIALITY IN

ENGLAND AND WALES
The first civil piece of legislation prohibiting bestiality was in 1533
enacted during the reign of Henry VIII with the title of: An Acte for the
punishment of the vice of Buggerie.34 Anyone found to have committed an
offence under the Act faced the punishment of death by hanging. In following
similar language as the 1533 Act, under the 1861 Offences Against the Person
Act, the “abominable” crimes of sodomy and bestiality were referred to as
“unnatural offences.” 35 The death penalty for sodomy and bestiality was
abolished and replaced with penal servitude for life or for any term not less
than ten years. While the bestiality provisions under the Offences Against the
Person Act 1861 still apply in Ireland, sections 61-63 were repealed in
England and Wales by virtue of the Sexual Offences Act 1956.36 Section 12 of
the Act provided for bestiality and reduced the punishment from life
imprisonment to two years. The 1956 Act was repealed by the Sexual
Offences Act 2003.
In 1999 the Home Secretary in the United Kingdom announced that a
review of sexual offences legislation would take place. A Committee was
convened by the Home Office in 2000 and the Committee published a report
33
The Local, “Denmark's bestiality ban moves forward.”
34
25 Henry VIII (1533), c. 6. This Act was repealed by the Offences against the Person Act 1828
(9 Geo.4 c.31).
35
24 & 25 Vict. c 100, Sections 61 to 63.
36
(c. 69), Schedule 4.
108 Laura Donnellan
entitled “Setting the Boundaries: Reforming the law on sex offences.” 37 In

contrast to the findings of Grassberger discussed above, the Committee (at
para. 5.8.3) stated:
“There is evidence of a linkage between abuse of animals and other

forms of sexual offending. Research has shown a link between abuse of
animals and abuse of children. In some instances, severe physical
mutilation of horses has been accompanied by sex with them. We felt that
society had a profound abhorrence for this behaviour and that it should
continue to be a criminal offence.”
In citing its agreement with the Criminal Law Revision Committee

(CLRC), the Committee contended that the criminal offence of bestiality
should remain albeit with a lesser penalty. The Committee did not refer to any
specific literature that demonstrated the link between other types of sexual
abuse. It would seem that it was merely conjuncture. The Committee
recommended that bestiality be placed under “compelling sexual acts” (at
para. 2.20.1). Under this category, the compellor forces others to engage in
sexual relations or may force an individual to perform sexual acts on the
compellor, or on or with an animal. The Committee (at para. 2.20.1)
concluded:
“The law should be able to state very clearly that compelling others
to do such acts against their will is an offence and that the guilt lies with
the person who compels the act rather than his or her immediate
victim.”38
While the Sexual Offences Bill 2003 was being debated, both the House
of Lords and Liberty make some very valid submissions. In the debate
preceding the Act it was suggested by Liberty (at paras. 17 and 18), the human
rights and civil liberties organisation, that bestiality should be addressed from
an animal welfare perspective and provided for under animal welfare
legislation. In looking at the issue from an animal welfare perspective, Liberty
contended that the welfare of animals “is of greater concern than the morality
of the sexual act” (at para.18). It questioned the restriction of the offence to
37
The full report can be accessed at: http://webarchive.nationalarchives.gov.uk/+/
http:/www.homeoffice.gov.uk/documents/vol1main.pdf?view=Binary.
38
See R v Bourne (1952) 36 Cr. App. R. 125.
only penetrative sex (vaginal or anal of the person or animal) and why it was
not extended to all forms of sexual acts involving an animal.
In the House of Lords, Lord Lucas questioned the insertion of provisions
relating to bestiality in the Sexual Offences Bill.39 He (at c574) referred to the
sexual predilections of many people which take place in private yet it “most of
us would find more or less disgusting. Intercourse with an animal is one of
them, but it is one which in some societies is considered normal.” Lord Lucas
referred to a study undertaking by Masters and Johnson where it was found
that bestiality was prevalent among juveniles living on farms in Ohio. He also
referred to the prevalence of pornography suggesting that the ubiquity of
bestiality and pornography had in some way contributed to their social
acceptance in some quarters of society. Lord Lucas (at c574) questioned the
Government’s motivation in including bestiality within the 2003 Bill, he
proffered that the motivation behind it had more to do with animal welfare as
opposed to the effect it had on humans. If the impetus behind the provisions
was animal protection, Lord Lucas asked whether the Minister had any
evidence to show the effect bestiality can have on the animal. Lord Lucas (at
c574) concluded by asking: “Why, among all human sexual perversions, is this
one chosen to make an offence?”
Lord Monson Crossbench (at c575) also questioned its inclusion
considering it is a very rare crime with a prosecution rate of less than one per
cent. Lord Falconer of Thoroton (at c575) responded to the questions raised by
Lord Lucas and Lord Monson. He referred to the fact that intercourse with an
animal was an offence under section 12 of the Sexual Offences Act 1956
which also included buggery and carried a maximum penalty of life
imprisonment. Section 12 was being repealed by the 2003 Bill. He explained
that a specific separate offence to cover bestiality was needed, one that was
distinct from those involving people. The proposed section on animals would
make the intentional penile, vaginal and anal penetration of an animal a crime
along with the causing or allowing the penis of a living animal to penetrate a
person’s vagina or anus. Lord Falconer (at c575) stated that such “behaviour is
generally accepted to be deviant” and did not have as its motivation the
protection of animal welfare, which he posited was dealt with in other statutes,
but that it should be a criminal offence. The new Act would reduce the penalty
as the 1956 Act prescribed a maximum punishment of life imprisonment,
which was deemed to be disproportionate (Lord Falconer, at c575). The Bill
proposed a maximum penalty of two years' imprisonment or a fine.
39
HL Deb, 19 May 2003.
110 Laura Donnellan
Lord Lucas (at c575) was not satisfied with the response provided by Lord
Falconer and questioned why it was only an offence if the animal was alive
and would it be less of an offence if the animal was killed in advance of the
sexual encounter. He also questioned the scope of the offence and why
penetration was required in order for it to be an offence. Lord Falconer (at
c575), in a similar vein to Richard Martin in the debates surrounding the 1822
Ill Treatment of Cattle Act and subsequent amendments, answered Lord Lucas
as follows:
“We have drawn the line where we have drawn the line. There is no
merit in saying that that is not this bad or that bad. What one has to do is
see where we have drawn the line and ask whether we have done that in
the right place.”
The Lords accepted the proposed amendments, however, returned to

Clause 72 as it was referred to, in a subsequent debate.40 Lord Lucas referred
to where Lord Falconer had “drawn the line” (at c81). The debate presented a
rare opportunity to examine the law relating to sexual contact and animals;
therefore there was a need to discuss the particular boundaries of the offence.
Clause 72 concerned the penetration by the human, however, what about
smaller animals being used in what Lord Lucas referred to as “fetching.” This
involves small animals, such as gerbils, being inserted in the anus or vagina in
order for the human to derive sexual pleasure. Lord Lucas (at c81) contended:
“I do not see the difference in the quality of the offence. If one is outrageous to
public decency in the public imagination, then it seems that the other one
should be too.” In returning to the omission of dead animals, Lord Lucas (at
c81) referred to “avisodomy” where the hen’s neck is broken just before
penetration in order to heighten the sexual pleasure of the human as the hen’s
neck spasms. In interpreting Clause 72 in its literal meaning, as the hen is dead
once penetrated no offence would be committed. Lord Lucas (at c82) was not
suggesting that all types of sexual contact be a criminal offence, such as
masturbation, however, he was questioning the logic of omitting dead animals.
Lord Lucas concluded (at c82):
“Leaving that aside, we ought to have boundaries which are drawn in

a reasonably logical place and which reflect the current practice of
bestiality, rather than something which perhaps has been drawn from a
40
HL Deb, 09 June 2003 vol. 649 cc47-116.
civil service cushioned from coming across these matters on a day-to-day

basis.”
Lord Monson (at c82) praised Lord Lucan’s research and while accepting
the arguments made, he reiterated the point of the Bill: to reduce the maximum
penalty of life imprisonment. He noted that decriminalisation of the offence
was not favoured, so a balance had to be struck. Where prosecutions had been
brought the average sentence was nine months under the existing legislation
with some offenders receiving non-custodial sentences (Lord Monson, at c82).
The proposed Bill would be legitimising an existing practice. Under the new
provisions, Lord Monson (at c82) contended that non-custodial sentences
would be the usual penalty except in situations involving animal cruelty. In
taking a holistic view of the offence, Lord Monson (at c82) opined that the
government had “broadly got it about right.” Lord Falconer (at c82) concurred
with Lord Monson and commended Lord Lucas on his research, he reiterated
the rarity of these offences and that the fact that animal welfare legislation
protected animals from cruelty and negligence. He (at c82) agreed with Lord
Monson that the government was correct and that Clause 72 as it was should
stand. Lord Lucas (at c83), conceding defeat, withdrew his amendment and
agreed to Clause 72 as it was.
The Sexual Offences Act 2003 received Royal Assent on the 20th of
November 2003. Bestiality is under section 69 which falls under “other
offences” along with: exposure (section 66), voyeurism (section 67), sexual
penetration of a corpse (section 70) and sexual activity in a public lavatory
(section 71).41 The text of section 69 is as follows:
(1) A person commits an offence if—

(a) he intentionally performs an act of penetration with his penis,
(b) what is penetrated is the vagina or anus of a living animal, and
(c) he knows that, or is reckless as to whether, that is what is penetrated.
(2) A person (A) commits an offence if—

(a) A intentionally causes, or allows, A’s vagina or anus to be penetrated,
(b) the penetration is by the penis of a living animal, and
41
Ss. 66-72 repealed (N.I.) (2.2.2009) by The Sexual Offences (Northern Ireland) Order 2008
(S.I. 2008/1769 (N.I. 2)), arts. 1, 78(e), Sch. 3; (with Sch. 2 para. 1) S.R. 2008/510, art. 2. The
offence of sex with an animal is found under section 73 of the 2008 Order and replicates the
text in section 69 of the 2003 Act.
112 Laura Donnellan
(c) A knows that, or is reckless as to whether, that is what A is being

penetrated by.
(3) A person guilty of an offence under this section is liable—

(a) on summary conviction, to imprisonment for a term not exceeding 6
months or a fine not exceeding the statutory maximum or both;
(b) on conviction on indictment, to imprisonment for a term not exceeding
2 years.
There are a number of pieces of legislation in England and Wales that

provide for sexual violence against animals, however, the definitions differ
(Pegg & Davies, at p.129). Under the 2003 Act only penetrative sex (vaginal
or anal of the person or animal) is a criminal offence. Oral penetration is
excluded. Under the Criminal Justice and Immigration Act 2008 section 63 it
is an offence to be in possession of extreme pornographic images and it
includes, under (7) (d), the offence of “a person performing an act of
intercourse or oral sex with an animal (whether dead or alive),” and a
reasonable person looking at the image would think that any such animal was
real. The inconsistencies undermine what little protection is provided for
animal victims of sexual assault. Perhaps a provision could be included in the
Animal Welfare Act 2006 that would make it an animal cruelty offence and
put the focus back on the welfare of animals and not about regulating human
morals.
The other issue is lack of reporting in England and Wales. Bestiality
seems more widespread in Denmark than in comparison to Ireland, England
and Wales. In a study conducted by the Danish Justice Ministry in 2011, 17%
of veterinary surgeons surveyed had treated an animal they suspected had
intercourse with a human.42 However, the figures in England and Wales could
be somewhat distorted. According to Home Office figures, in 2010/2011 only
12 “unnatural sexual offences” were recorded (Brayford, Cowe & Deering, at
p.154). Sexual penetration with a corpse was included in the 12 recorded
offences. There is no requirement of veterinary surgeons to report any
suspected cases to the authorities. Members of the public are also reluctant to
report to the police. The victim, the animal, cannot make a complaint. In
England and Wales, the Royal Society of the Prevention of Cruelty to Animals
(RSPCA) is not always aware that an animal has been subjected to sexual
42
Reuters. UPDATE 1-Denmark bans bestiality in move against animal sex tourism.
intercourse when officers are inspecting suspected cases of cruelty. Offences

of this nature are very much taboo.
THE LAW RELATING TO BESTIALITY IN IRELAND

While laws around the European Union have been updated in relation to
bestiality, the offence of bestiality in Ireland is governed by Offences Against
the Person Act 1861, sections 61-63. Until the Criminal Law (Sexual
Offences) Act 1993, bestiality and buggery between humans were seen as
equivalent offences and categorised as “unnatural offences.” Homosexuality
was decriminalised by virtue of section 2 of the 1993 Act. As noted above,
prior to the removal of buggery, section 61 prohibited sodomy and bestiality
and provided a sentence of penal servitude for life or any term not less than ten
years. Section 62 provided that anyone attempting or intending to commit
either sodomy (or any indecent assault upon any male person) or bestiality
were guilty of a misdemeanour with the court being endowed with the
discretion to sentence the offender for up to ten years but not less than three
years of penal servitude or imprisonment for any term not exceeding two years
with or without hard labour. Section 63 defined carnal knowledge to mean
penetration only and ejaculation (“Emission of Seed”) was not needed to prove
that an offence had been committed.
Under paragraph 9 of the Schedule of the Sex Offenders Act 2001,
“Sexual offences for the purposes of the Act” includes the offence of buggery
with a person or with an animal as referred to in section 61 of the Offences
Against the Person Act 1861. Under paragraph 10, the offence of an attempt to
commit such buggery as denoted in section 62 of the Act of 1861 is also
referred to. While the 1993 Act abolished the offence of buggery between
persons, O’Malley (at p.126) opines that “buggery in the form of intercourse
with an animal (bestiality) was thereby left intact, although these offences are
exceedingly rare.”
Unlike the Sexual Offences Act 2003 (England and Wales), the Irish
legislation refers only to buggery and there is no mention of vaginal
penetration between a female human and male animal nor penetration by a
human male of a female animal. However, in a case from December 2012
presided over by Judge Carroll Moran in Limerick Circuit Court, there was
vaginal penetration of a woman who had sexual intercourse with a German
Shephard. The woman died subsequently in a hospital. The owner of the dog
was charged under the 1861 Act and was given a three year suspended
114 Laura Donnellan
sentence (section 62), despite, in the words of Judge Moran, “the disgusting
nature of the offence.” The male offender’s name was put on the Sex
Offenders’ Register for five years. The maximum penalty the man faced was
life in prison under section 61. The male offender was charged with buggery
even though it was the woman who had sexual intercourse with the dog. A
DNA test from the semen obtained from the deceased was shown to come
from the German Shephard. An aggravating factor for the Court was the fact
that the owner of the dog had accessed a bestiality website which had over 1.5
million hits on his laptop over a five-month period. Judge Moran referred to
the facts of the case as “socially repugnant . . . even in these tolerant times”
(Hayes). The offender, a bus driver, was restricted from driving a bus for five
years under European Union law which was incorporated into national law.43
The Regulations prohibit a convicted sex offender from operating a vehicle
with over nine persons including the driver. As the willing participant had
passed away and thus was not charged with an offence, it would seem that
vaginal penetration would fall within the definition of buggery for the
purposes of section 61 of the 1861 Act. Although of persuasive authority, the
English case of R v Bourne is instructive as it involved vaginal penetration of a
dog by the appellant’s wife who was under duress and thus lacked the
necessary mens rea.44 Had the wife been a willing participant she would have
been convicted. The appellant was found to be a principal in the second degree
crime of buggery and an aider and abettor. Although section 61 refers to
buggery, it would arguably also include vaginal penetration under Irish law.
Ireland overhauled its animal welfare legislation in 2013 under the Animal
Health and Welfare Act 2013, which commenced on the 6th of March 2014.
The principle Act until this was the Protection of Animals Act 1911. 45 In
adapting a similar provision as to the five freedoms of the English and Welsh
2006 Act, section 11(1) of the 2013 Act enumerates the responsibilities of
those in possession or those who have a protected animal46 under his or her
control: “having regard to the animal’s nature, type, species, breed,
development, adaptation, domestication, physiological and behavioural needs
and environment, and in accordance with established experience and scientific
knowledge, take all necessary steps to ensure that—
43
S.I. No. 318/2009 - European Communities (Road Haulage and Road Passenger Transport
Operator’s Licences) Regulations 2009.
44
(1952) 36 Cr. App. R. 125.
45
c. 27.
46
A protected animal is defined as: a) kept for farming, recreational, domestic or sporting
purposes in the State, (b) when it is in the possession or under the control of a human being
whether permanently or on a temporary basis, or (c) that is not living in a wild state.
(a) the animal is kept and treated in a manner that—

(i) safeguards the health and welfare of the animal, and
(ii) does not threaten the health or welfare of the animal or another
animal.”
A person who fails to comply with section 11 (1) is guilty of an offence

under section 11 (2). Section 12 lays out the provisions concerning the
prohibition of animal cruelty and makes it an offence to subject a protected
animal to unnecessary suffering or to neglect, or be reckless, regarding the
health or welfare of an animal. Section 12 (4) provides a number of
considerations in relation to unnecessary suffering:
(a) whether the suffering could reasonably have been avoided,

terminated or reduced,
(b) whether the conduct which caused the suffering was in
compliance with this Act, another enactment, animal health and welfare
regulations or a code of practice,
(c) whether the conduct which caused the suffering was for a
legitimate purpose, such as—
(i) benefiting the health and welfare of the animal, or

(ii) protecting a person, property or another animal,
(d) whether the suffering was proportionate to the purpose of the

conduct concerned, and
(e) whether the conduct concerned was in all the circumstances that
of a competent and humane person.
Arguably, bestiality could fall under sections 11 and 12. Under section 11,
bestiality could be included under: “physiological and behavioural needs and
environment” and under section 12 it could be deemed a form of animal
cruelty. It would be very difficult to justify bestiality as having a legitimate
purpose or benefitting the health and welfare of the animal or protecting a
person, property or other animal. However, if bestiality were to be implied,
subsection (e) could be used by those who contend that bestiality should not be
seen as a criminal offence but rather a mental illness that requires psychiatric
treatment.
The inclusion of sexual intercourse with an animal would have put animal
welfare to the forefront. However, given the rarity of prosecutions, it may be
viewed as superfluous and unnecessary.
116 Laura Donnellan
RECOMMENDATIONS AND CONCLUSION

As the above discussion demonstrates, laws relating to bestiality espouse
an anthropomorphic view, with the focus being on the effect that bestiality has
on society as opposed to the effect it can have on an animal. It is seen as an
abasement of the individual that can lead to other sexual offences, in particular
the abuse of children and other vulnerable persons. The word bestiality
conjures up images of beasts, modern discourse has moved away from such
language to refer to animals as sentient beings with some writers taking
umbrage to the word animal and instead referring to them as non-humans (for
example Tom Reagan). Singer refers to persons and non-persons instead of
using the terminology humans and non-humans.
Bestiality should be referred to as animal sexual abuse and by referring to
it as bestiality or zoophilia the law sanitises the offence. It places the human at
the forefront and marginalises the effect it has on the animal. Bestiality is seen
as a degradation of the person that evokes feelings of disgust and revulsion
among the public. Sexual abuse of animals could be included within the
parameters of animal welfare legislation under the definition of cruelty. The
common law definition which criminalises penetration could be extended to
include all forms of sexual relations including oral sex. While the eating of
meat and the use of animals in science can be justified by an overriding public
interest, the sexual abuse of animals has no societal benefit. While the harm
principle, the offence principle, consent, legal paternalism and the legal
regulation of morals have been put forward as arguments in favour of the
criminalisation of bestiality, each one has a number of flaws which undermine
the encroachment of the legislature. When coming from an anthropomorphic
basis, animal welfare will always be a secondary consideration if even a
consideration.
By reclassifying bestiality as animal sexual abuse would put the focus
back on the welfare of animals and not about regulating human morals. By
placing bestiality within the confines of animal welfare legislation, the
argument in relation to consent being irrelevant (as animals are used by
humans for another of purposes, among them meat, clothing, hunting etc. and
arguably do not consent to such uses) can be removed from the discourse. A
duty of care should be placed on the person responsible for the animal that the
animal is not subject to sexual interference.
While Canada, Denmark, England and Wales have all updated their
legislation, the Offences Against the Person Act 1861 is still applicable in
Ireland. The 1861 Act is a bastion from the reign of Queen Victoria. Ireland
overhauled its animal welfare legislation in 2013 under the Animal Health and
Welfare Act 2013. The inclusion of sexual intercourse with an animal would
have put animal welfare to the forefront. The argument that bestiality is a
“gateway offence” and may lead to the abuse of vulnerable persons including
children means that the offence should not be taken lightly. However, under
Irish law children are already protected under the Sexual Offences Act 2006
and in the future when the current Bill, the Criminal Law (Sexual Offences)
Bill 2015 becomes law. An amendment to the Animal Health and Welfare Act
2013 might be the most prudent way to deal with the issue of sexual
intercourse and the sexual abuse of animals in Ireland.
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Phenomenon Between Crime, Paraphilia and Love. Journal of Forensic
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Antonio M. Haynes. (2014-2015). The Bestiality Proscription: In Search of a
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Debates and New Directions. Oxford: OUP.
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118 Laura Donnellan
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1824), cc.865-69.
Colin J. Williams & Martin S. Weinburg. (2003). Zoophilia in Men: A Study
of Sexual Interest in Animals. Archives of Sexual Behaviour, 32 (6), 523-
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Dennis J. Baker. (2016). The Right Not to be Criminalised Demarcating
Criminal Law’s Authority. London and New York: Routledge.
Frank R. Ascione (with Phil Arkow). (1999). Child Abuse, Domestic Violence,
and Animal Abuse: Linking the Circles of Compassion and for Prevention
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Gary L. Francione. (1995). Animals, Property and the Law. Philadelphia:
Temple University Press.
H. Montgomery Hyde. (1970). The Love That Dared Not Speak Its Name: A
Candid History of Homosexuality in Britain. Boston: Little, Brown.
Home Office (2000) Setting the Boundaries: Reforming the law on sex
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publications.parliament.uk/pa/ld200203/ldhansrd/vo030609/text/30609-
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Imogen Jones. (2011). A beastly provision: why the offence of ‘intercourse
with an animal’ must be butchered. Journal of Criminal Law, 75 (6), 528-
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J. Paul McCutcheon. (2002). Morality and the Criminal Law: Reflections on
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John Stuart Mill (1865) On Liberty. Longmans, Green, and Company.
Kathryn Hayes. (2012). Suspended three-year sentence for man's role in
bestiality act, Irish Times, http://www.irishtimes.com/news/suspended-
three-year-sentence-for-man-s-role-in-bestiality-act-1.3124, published
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Kent Greenawalt. (1973). Legal Enforcement of Morality. The Journal of
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Laura Donnellan. (2008). The effect of recent developments in animal welfare

on international trade and commerce. Commercial Law Practitioner 15
(5), 103-112.
Liberty. (2003). Liberty’s second reading briefing on the Sex Offences
(Amendment) Bill in the House of Commons, July, 2003. Available at:
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bill-2nd-reading-commons.pdf.
Margaret Thornton. (1997). The Judicial Gendering of Citizenship: A Look at
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Merck, ed.) Veterinary Forensics: Animal Cruelty Investigations. (pp233-
241). 2n ed., Ames, Iowa: Wiley-Blackwell.
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Why the Laws in Opposition Can Find No Support in the Harm Principle,
The Jurisprudence of Bestiality. Journal of Animal and Environmental
Law, 1, 176-221.
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(London: T.C. Hansard, 1809).
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Piers Beirne. (2001) Peter Singer's ‘Heavy Petting'' and the Politics of Animal
Sexual Assault.’ Critical Criminology 10, 43-55. DOI: 10.1023
/A:1013119904480.
120 Laura Donnellan
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sex tourism, http://www.reuters.com/article/denmark-bestiality-idUSL5N
0XI3A020150421, published online on February, 21, 2015.
Robert L. Crooks & Karla Baur. (2015). Our Sexuality. 13th ed., Boston:
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Basic Writings of Saint Thomas Aquinas. New York: Random House.
Samantha Pegg & Anne Davies. (2016). Sexual Offences: Law and Context.
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353/8022609.htm.
Shaunnagh Dorsett. (1998). Land Law and Dispossession: Indigenous Land
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Eykyn Hovenden, Archer Ryland. (1853). Commentaries on the Laws of
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Publisher.
Steven White. (2009). Exploring Different Philosophical Approaches to
Animal Protection Law. In (eds. Peter Sankoff & Steven White), Animal
Law in Australasia (pp.79-107). Sydney: Federation Press.
Stine B. Christiansen, PhD, University of Copenhagen and The Danish
Council for Animal Ethics (2014) ScienceNordic, “Denmark moves to ban
bestiality -- but is sex with animals really so bad? http://sciencenordic
.com /denmark-moves-ban-bestiality-sex-animals-really-so-bad, published
online on October, 16, 2014.
The Local. (2014). Bestiality ban not needed: Ethics Council.
http://www.thelocal.dk/20141013/bestiality-ban-not-needed-ethics-
council-says, published online on October, 13, 2014.
The Local. (2015). Denmark's bestiality ban moves forward.

http://www.thelocal.dk/20150225/denmarks-bestiality-ban-moves-
forward, published online on February, 25, 2015.
Thomas O’Malley. (2013). Sexual Offences. 2nd ed., Dublin: Roundhall.
Tom Reagan. (2004). The Case for Animal Rights. Los Angeles: University of
California Press.
BIOGRAPHICAL SKETCH
Laura Donnellan
Affiliation: Lecturer in Law, School of Law, University of Limerick
Education: LLB, LLM, PhD. Candidate
Business Address: School of Law, University of Limerick, Castletroy,

Limerick, Ireland.
Research and Professional Experience: Laura Donnellan teaches

European Union Law, Sport and the Law and Comparative Property Law. She
has published in the areas of drug testing and the rights of athletes, elder law,
the regulation of football agents, TV rights in Irish football, EC competition
law, horse racing and animal welfare and animal welfare in the EU. She
graduated with an LLM from the University of Limerick in 2002. Laura is the
author of Sport and Law A Concise Guide (Blackhall Publishing 2010) as well
as a number of articles in international law journals. She is an Associate
Fellow at the Oxford Centre for Animals Ethics and a Consulting Editor for
the Journal of Animal Ethics (published by the University of Illinois). Laura is
currently an external examiner on the LLB programme for the Dublin
Business School. She has co-written Sports Law in Ireland (with her colleague
Dr. Susan Leahy) published by Kluwer. The second edition of Sports Law in
Ireland will be published in the latter part of 2016.
Professional Appointments: External Examiner Dublin Business School

122 Laura Donnellan
Publications:
Book: Sports Law in Ireland (with Dr. Susan Leahy) (The Hague, Kluwer,
2014).
Chapter: “R v Countryside Alliance” (pp.337-352) In Contribution to
Landmark Cases and Decisions in Sports Law (Asser Press, The Hague, 2013)
(edited by Prof. Jack Anderson).
Articles: “Dispute Resolution in Irish Sport: The Courts as Reluctant
Interlopers” (2016) 14 (1) Entertainment and Sports Law Journal 1–15, DOI:
http://dx.doi.org/10.16997/eslj.195.
“Fox hunting and developments in the nineteenth and twentieth century:
part one” (2015) 1 Global Sports Law and Taxation Reports 31-34.
“Fox hunting and developments in the nineteenth and twentieth century:
part two” (2015) 2 Global Sports Law and Taxation Reports 14-18.
“A Storm in a Tea Cake? Lees of Scotland Ltd &Thomas Tunnock Ltd v.
HMRC” (2014) 35 (5) Business Law Review 181-184.
“The transfer of race horses between the United Kingdom, Ireland and
France: the 2014 Reforms” (2014) 3 (1) Global Sports Law and Taxation
Reports 19-21.
Blogs: “The transfer of race horses between the United Kingdom, Ireland
and France,” The Economics of Sports, 22nd April 2014, http://www.sports
economics.org/2/post/2014/04/the-transfer-of-race-horses-between-the-united-
kingdom-ireland-and-france.html.
“Laura Donnellan of the University of Limerick an Expert on Equestrian
Law Comments on the Godolphin New Market Racing Stables Horse Doping
Scandal!” SportsandTaxation.com http://www.sportsandtaxation.com/2013/04/
laura-donnellan-of-the-university-of-limerick-an-expert-on-equestrian-law-
comments-on-the-godolphin-new-market-racing-stables-horse-doping-
scandal/.
“Racing.com’s acquisition of rights to broadcast Hong Kong racing: A
False Start?” Sports and Taxation.com, http://www.sportsandtaxation.com/
2016/06/racing-coms-acquisition-of-rights-to-broadcast-hong-kong-racing-a-
false-start/.
“Godolphin and Under Armour: Historic Sports Marketing Partnership”
Sports and Taxation.com, http://www.sportsandtaxation.com/2016/04/
godolphin-and-under-armour-historic-sports-marketing-partnership/.
Guest Blog – “Mixed Martial Arts (MMA): Legal Issues by Laura
Donnellan,” Asser International Sports Law Blog, http://www.asser.nl/Sports
Law/Blog/post/guest-blog-mixed-martial-arts-mma-legal-issues-by-laura-
donnellan.
“32Red Sponsors British Horseracing: Do Betting Companies Undermine
the Corinthian Ideals of Sport?” Sports and Taxation.com,
http://www.sportsandtaxation.com/2016/09/32red-sponsors-british-
horseracing-do-betting-companies-undermine-the-corinthian-ideals-of-sport/
Chapter 4
ANIMAL WELFARE IN THE EUROPEAN

UNION’S EXTERNAL RELATIONS LAW
Yumiko Nakanishi *
Hitotsubashi University, Tokyo, Japan
ABSTRACT
Animal welfare is an important issue in European Union (EU)
Article 13’s Treaty on the Functioning of the European Union (TFEU).
The EU has taken measures toward animal welfare. Some of those
measures have influenced third countries or have been criticized by other
countries. For example, an EU measure banning seal product imports
became a point of conflict between the EU and Canada in the World
Trade Organization (WTO). On the other hand, the EU has concluded and
is negotiating free trade agreements (FTAs) with third countries. Animal
welfare is regulated in those agreements, based on input from civil
societies and non-governmental organizations (NGOs). This article aims
to analyze from a legal perspective the EU’s measures and strategies for
animal welfare in its external relations and to highlight the development
of the concept of animal welfare in the EU and in its relationships with
the rest of the world.
*
Yumiko.nakanishi@r.hit-u.ac.jp.
126 Yumiko Nakanishi
1. INTRODUCTION
The European Economic Community (EEC) started with the Roman
Treaty, which was signed in 1957 and entered into force in 1958. The aim of
the EEC was economic integration, specifically the establishment of a
common market including a customs union. At that time, animals were
considered agricultural products1. The EEC became the European Community
(EC) with the Treaty on the European Union (EU) and the Treaty of
Maastricht, which was signed in 1992 and entered into force in 1997. This
meant that the aim of the Community was not only economic integration, but
also integration in other fields. Furthermore, the Treaty of Lisbon was signed
in 2007 and entered into force on December 1, 2009. The Treaty of Lisbon
abolished the EC and established the EU in its place. The current EU is
founded on the Treaty on the EU (TEU) and the Treaty on the Functioning of
the EU (TFEU), based on the Treaty of Lisbon.
The Union’s aim is to promote peace, its values, and the well-being of its
people (Article 3 TEU). According to the Treaty of Lisbon, the EU now has
their own values: respect for human dignity, freedom, democracy, equality, the
rule of law and respect for human rights (Article 2 TEU). Animal welfare is
also considered among the Union’s values. Article 13 TFEU considers animals
to be sentient beings. This provision reflects a new concept of animals for the
Union and its Member States, and this concept began to influence third
countries through EU measures reflecting it (for example, the EU bans on
trade in seal products and cosmetic products tested on animals).
This chapter shows the uniqueness and progressiveness of the Union’s
measures regarding animal welfare. First, it explains the historical
development of animal welfare in the EU in the context of the development of
European integration, comparing it to the Union’s environmental policies
including those for animal protection. Second, we will examine why the
measures for animal welfare were developed. Third, we explain the Union’s
external policies and principles. Finally, we describe concrete cases related to
animal welfare in the Union’s external activities, including WTO conflicts and
Free Trade Agreements between the EU and third countries.
1
Lennkh, S. (2010), Die Kodifikation des Tierschutzrechts, Nomos, p. 120.
Animal Welfare in the European Union’s External Relations Law 127
2. THE HISTORICAL DEVELOPMENT

OF ANIMAL WELFARE
2.1. From Economic Integration Toward De-Economic

Integration
The aim of the EEC was economic integration, specifically the

establishment of the Common Market. At the time of the establishment of the
EEC in 1958, there was no reference to environmental protection in the EEC
Treaty. However, at the summit of 1972, European leaders agreed to take
action to protect the environment. After the summit, the Community began to
take measures related to the environment. There was no explicit individual
legal basis for environmental protection in the EEC Treaty, but the
Community used Article 100 TEEC (now Article 115 TFEU) and 235 TEEC
(now 352 TFEU) for this purpose. Article 100 TEEC formed the legal basis for
the Common Market, and Article 235 TEEC was the legal basis for attaining
the objectives of the Community. A major change was the Single European
Act (SEA), which was signed in 1986 and entered into force in 1987. The SEA
conferred to the Community explicit competence to legislate measures for
environmental policy (Article 130t TEEC (now Article 192 TFEU)). After the
SEA, environmental protection became one of the objectives of the
Community. This meant the aim of the Community was no longer only
economic integration, but integration in other domains, including the
environment.
The Union works “for the sustainable development of Europe…, aiming at
a high level of protection and improvement of the quality of the environment”
(Article 3 TEU). The EU has four environmental principles (Principle of
Prevention, Source Principle, Precautionary Principle and Polluter Pays
Principle) (Article 191 paragraph 2 TFEU)2. Title XX of Part Three, “Union
Policies and Internal Actions” of TFEU is environment. Title XX comprises
Articles 191~193 TFEU. Article 191 TFEU is the current version of Article
130r TEEC, which was introduced by the SEA. Article 191 TFEU lays down
the four following objectives of the Union’s environmental policy: (1)
preserving, protecting, and improving the quality of the environment; (2)
protecting human health; (3) prudent and rational utilization of natural
2
Proelss, A. (2016), “Principles of EU Environmental Law: An Appraisal,” In Y. Nakanishi
(ed.), Contemporary Issues in Environmental Law, Springer, pp. 29-45; The EU tends to insist
the introduction of the precautionary principle at international stage.
resources; and (4) promoting measures at the international level. Because there
is no definition of “environment,” the concept of the environment has been
broadly interpreted. Article 191 TFEU (former Article 130r TEEC) does not
refer to animals, but measures related to animals have been adopted, such as
the Birds Directive3 and the Habitats Directive4. Those directives serve as the
two pillars of nature conservation policy5.
2.2. The Development of the Provision for Animal Welfare
Protection of animals as part of environmental policy differs from animal

welfare. Animals are protected in the context of environmental policy when
animals are endangered species. Animal welfare, in contrast, should be
considered even for animals that are not endangered.
Environmental measures began with the Paris summit in 1972 as
mentioned above. Measures for animal welfare did not entail as dramatic a
change. Measures on animal welfare were found in the 1970’s in the Union’s
agricultural policy 6 . For example Directive 74/577/EEC on the stunning of
animals before slaughter was adopted in 1974 based on Article 43 TEEC (now
Article 43 TFEU)7. According to the measure, all forms of cruelty to animals
and all unnecessary suffering of animals were to be avoided.
Although there were already measures for animal welfare in the 1970’s,
there were no provisions for animal welfare in the TEEC. However, there has
been a provision for animals since the TEEC. Article 36 TEEC (now Article
36 TFEU) states, “the provisions of Articles 34 and 35 shall not preclude
prohibitions or restrictions on imports, exports, or goods in transit justified on
grounds of public morality, public policy, or public security; the protection of
health and life of humans, animals or plants….” This means that protection of
3
OJ of the EU 2010 L20/7, Directive 2009/147/EC of the European Parliament and of the
Council of 30 November 2009 on the conservation of wild birds.
4
OJ of the EU 1992 L206/7, Directive 92/43/EEC on the conservation of natural habitats and of
wild fauna and flora.
5
Ex. De Vido, S. (2016), “Protecting Biodiversity in Europe: The Habitats and Birds Directives
and Their Application in Italy in an Evolving Perspective,” In Y. Nakanishi (ed.),
Contemporary Issues in Environmental Law, Springer, p.115, p. 118.
6
Nakanishi, Y. (2016), “The Principle of Animal Welfare in the EU and Its Influence in Japan
and the World,” In Y. Nakanishi (ed.), Contemporary Issues in Environmental Law, Springer,
p. 87, pp. 88-91.
7
OJ of the EU 1977 L316/10.
the health and life of animals can be cited to justify national restrictions on
trade8.
Animal welfare in the EU developed with the Treaties 9 . First, the
Maastricht Treaty annexed protocols and declarations, one of which stated that
the governmental conference required EU institutions and Member States to
fully consider the welfare requirements of animals when drafting and
implementing Community measures on common agricultural policy, transport,
and the internal market. This was a “soft” integration clause 10 . Second, a
protocol annexed to the Treaty of Amsterdam 11 was the Protocol on the
Protection and Welfare of Animals. While declarations are not legally binding,
protocols are, and the Protocol specifies, “…In formulating and implementing
the Community’s agriculture, transport, internal market, and research policies,
the Community and the Member States shall pay full regard to the welfare
requirements of animals….” This effectively strengthened animal welfare in
the EU. Furthermore, the Treaty of Lisbon introduced a new provision for
animal welfare in Article 13 TFEU. Article 13 TFEU specifies the following:
“In formulating and implementing the Union’s agriculture, fisheries,
transport, internal market, research and technological development, and space
policies, the Union and the Member States shall, since animals are sentient
beings, pay full regard to the welfare requirements of animals….”
Although the provision is weak compared to Article 11 TFEU in its
environmental integration clause, the force of the article on animal welfare in
the TFEU is meaningful12. It shows the new idea that animals are not goods,
but sentient beings that feel pain. The EEC originated with economic
integration, but the EU is no longer a purely economic union. The Union’s
environmental policy started with anthropocentrism. However, the Union now
considers the welfare of animals in part from the perspective of the animals.
This is a big step toward a higher ethic. Article 13 TFEU provides the EU with
a legal base (evidence) that represents the Union’s own values about animal
welfare to third countries.
8
Edward, D. & Lane, R. (2013), Edward and Lane on European Union Law, Edward Elgar, pp.
464-470, pp. 627-628 and footnote 825.
9
Nakanishi, Y. (2016), pp. 92-93.
10
Edward, D. & Lane, R. (2013), Edward and Lane on European Union Law, Edward Elgar, p.
419 (7.18).
11
The Treaty of Amsterdam was signed in 1997 and entered into force 1999.
12
Epiney, A. (2013), Umweltrecht der Europäischen Union, 3. Aufl., Nomos, p. 49 and p. 159.
3. SUPPORTING FACTORS PROMOTING

ANIMAL WELFARE
3.1. Public Opinion
The European Commission makes proposals for the EU measures. The

Commission has opportunities to consider public opinion13 when making its
proposals. Public participation in decision-making is important in the field of
animal welfare as well as in the field of environment 14. The Lisbon Treaty
amended the TEU and strengthened democracy. For example, Article 10,
paragraph 3 TEU rules that every citizen shall have the right to participate in
the democratic life of the Union, and decisions shall be made as openly as
possible with the greatest possible input from citizens. Article 11 TEU states
these conditions as follows:
“1. The institutions shall, by appropriate means, give citizens and

representative associations the opportunity to make known and publicly
exchange their views of all areas of Union action.
2. The institutions shall maintain an open, transparent, and regular
dialogue with representative associations and civil society.
3. The European Commission shall carry out broad consultations with
parties concerned in order to ensure that the Union’s actions are coherent and
transparent…”
Consideration for public opinion by the European Commission originated

with a white paper on European governance in 200115. Those practices by the
Commission are now regulated by the TEU. Dialogue with civil society can be
found not only in the Commission, but also in other EU institutions.
The EU measures regarding animal welfare are supported by public
opinion. The Commission published a community action plan on the
protection and welfare of animals 2006-2010 in 200616. The COM document
reported that the Action Plan on Animal Welfare was the subject of wide
13
For non-institutional actors, see Krämer, L. (2015), EU Environmental Law, 8 th Ed., Sweet &
Maxwell, 2015, pp. 48-51.
14
Cf. Shelton, D. (2006), “Human Rights and the Environment: What Specific Environmental
Rights Have Been Recognized?,” Denver Journal of International Law & Policy, Vol. 35(1), p.
129, pp. 130-131 and p. 139.
15
COM (2001) 428, European Governance: A White Paper.
16
COM (2006) 13, Communication on a Community Action Plan on the Protection and Welfare
of Animals 2006-2010.
public consultation in accordance with the Commission’s interactive policy

making 17 . The Commission stated that animal welfare policies need to be
founded on the best available scientific evidence and take into account public
concerns 18 . The Commission then published a COM document on the EU
strategy for the protection and welfare of animals 2012-2015 in 201219. In that
document, the Commission proposed to provide consumers and the public
with appropriate information, saying that animal welfare is a society-wide
concern that appeals to a wide portion of the public and is also a consumer
concern20.
The Commission proposed the regulation of trade in seal products on July
23, 200721. As part of the proposal’s grounds and objectives, the Commission
noted that for several years, many in the public had expressed moral concerns
about the killing and skinning of seals 22 , so the killing of baby seals,
particularly in Canada, attracted attention in Europe23. The Commission added
that it had received a massive number of letters and petitions expressing
citizens’ deep indignation and repulsion about the trade in seal products. Thus,
the public’s growing awareness and sensitivity to ethical considerations in how
seal products are obtained led the Commission to make its proposal 24 . The
proposal was adopted by the European Parliament and the Council on
September 16, 2009 as Regulation 1007/2009. Paragraph 4 of the preamble of
the regulation recognizes that “the hunting of seals has led to expressions of
serious concerns by members of the public and governments sensitive to
animal welfare considerations due to the pain, distress, fear, and other forms of
suffering which the killing and skinning of seals, as they are most frequently
performed, cause to those animals”25.
The Commission gives the public opportunities to voice their opinions,
and makes proposals based on these opinions. In Europe, NGOs and
consumers have been concerned about animal welfare, which has influenced
the governments of the Member States and the EU institutions.
17
COM (2006) 13, p. 2.
18
COM (2006) 13, p. 4.
19
COM (2012) 6, Communication on the European Union Strategy for the Protection and
Welfare of Animals 2012-2015.
20
COM (2012) 6, p. 5 and p. 10.
21
COM (2008) 469, Proposal for a regulation of the European Parliament and of the Council
concerning trade in seal products.
22
COM (2008) 469, p. 2.
23
Krämer, L. (2015), p. 219.
24
COM (2008) 469, p. 3.
25
OJ of the EU 2009 L286/36, Regulation 1007/2009 on trade in seal products.
3.2. The European Parliament
Attempts by animal welfare groups, supported by the EP, to incorporate a

specific provision on animal welfare into the EU Treaties succeeded with the
Treaty of Lisbon26. Thus, the EP played a role in introducing Article 13 TFEU.
The EP also supports animal welfare in other ways.
The Commission makes proposals. The European Parliament (EP) decides
on these proposals with the Council of the EU according to the ordinary
legislative procedures in Article 289 TFEU. At the beginning of the European
Community (now Union), the EP was just a consultative, rather than
legislative organ. However, the EP earned democratic legitimacy after the
introduction of direct universal suffrage in a free and secret ballot in June
1979. The powers of the EP have strengthened with several amendments of the
basic Treaties.
After the Treaty of Lisbon, the EP became the legislative organ of the
Council. In principle, EU measures are adopted by the co-decision of the EP
and the Council. In the past, the Council made its decisions based on the
proposals of the Commission after consultation with the EP. After the Treaty
of Lisbon, almost no measures could be adopted without the agreement or
consent of the EP. In the common commercial policy (CCP), the Council had
formerly adopted regulations and finalized agreement with third countries or
international organizations independently (Article 113 TEEC, Article 133
TEC). However, the Council now can adopt regulations only with the EP and
cannot conclude agreements without the consent of the EP, even in the CCP in
Article 207 TFEU. This means the Commission and the Council cannot ignore
debates and opinions in the meetings of the EP.
The number of the EP members (MEP), who serve as representatives of
EU citizens, is 751. In the EP are more than twenty committees including the
Environment Committee, Public Health and Food Safety Committee, and the
Internal Trade Committee, which address these respective issues. Additionally,
the EP has an intergroup on the Welfare and Conservation of Animals27, which
is open to all MEPs eager to debate and promote issues regarding animal
welfare, and brings citizens’ concerns about animal welfare to the attention of
MEPs.
In addition, the EP does not have the right of initiative to make legislation,
but the EP may request that the Commission submit any appropriate proposals
26
Krämer, L. (2015), p. 217.
27
http://www.animalwelfareintergroup.eu/about-us.
on matters that it considers for implementing the Treaties (Article 225 TFEU).
For example, the proposal of the Regulation 1007/2009 concerning trade in
seal products (which will be discussed below) was requested by the EP
(Preamble (1) of Regulation 1007/2009)28.
EU citizens and the EP support and encourage active measures by EU
institutions. Measures about animal welfare are becoming stronger and more
numerous in the EU.
4. UNION PRINCIPLES IN EXTERNAL ACTIONS

The Treaty of Lisbon specifies the Union’s values in Article 2 TEU, and
the activities of the Union are based on these values. If a European country
wants to be a Member State of the Union, it is obliged to accept those values
(Article 48 TEU). Member States must also respect those values. If a Member
State fails to comply with them, the Council may decide to suspend some of its
rights deriving from the application of the Treaties to the Member State,
including its voting rights and rights of representative in the government of the
Member State in the Council (Article 7 TEU). On the other hand, Article 21
TEU establishes the political principles for the EU’s external actions. Those
principles are democracy, the rule of law, the universality and indivisibility of
human rights and fundamental freedoms, respect of human dignity, the
principles of equality and solidarity, and respect for the principles of the
United Nations Charter and international law. The Union seeks to develop
relationships and build partnerships with countries that share those values and
principles, striving for an “ethical” foreign policy29.
Article 21 paragraph 2 (f) TEU specifies that the Union defines and
pursues common policies and actions and works for high degrees of
cooperation in all fields of international relations to help develop international
measures to preserve and improve the quality of the environment and the
sustainable management of global natural resources, in order to ensure
sustainable development. Furthermore, Article 21 paragraph 3 subparagraph 2
TEU states that the Union ensures consistency between the different areas of
its external actions and between these and its other policies.
28
Regulation 1007/2009 of the European Parliament and of the Council of 16 September 2009 on
trade in seal products, OJ 2009 L286/36.
29
Bartels, L. (2015),“Human Rights and sustainable development obligations in EU free trade
agreements,” In J. Wouters, A. Marx, D. Geraets, B. Natens, Global Governance through
Trade, Edward Elgar, pp. 73-91.
The Union’s values and principles are integrated into the EU’s measures
and actions. The Union’s internal policies and measures are connected with the
Union’s external policies and measures. Animal welfare is not directly referred
as one of the Union’s values or principles. However, the Union and the
Member States are obliged to fully consider the welfare requirements of
animals when formulating and implementing the Union’s policies because it
considers animals as sentient beings. This concept applies to the Union’s
internal and external policies and measures, and will be discussed in the next
chapter.
5. CONCRETE CASES
5.1. Measures in the EU
(1) Internal Measures

The Union takes measures to achieve the objectives established in the
Treaties. The EU can adopt regulations, directives, and decisions as ruled in
Article 288 TFEU. A regulation has a general application, is binding in its
entirety, and directly applicable to all Member States. A directive is binding
upon each Member State to which it is addressed in terms of the results to be
achieved, but national authorities have the choice of form and method of
implementing it. In the CCP, the EP and the Council can only adopt
regulations because unified application of the measures is necessary. In
contrast, for the Union’s environmental policies, directives are preferred over
regulations because they respect national differences. However, they also raise
compliance issues.
(2) External Measures

Generally, it is necessary for an international organization to conclude
agreements that the Organization has a legal personality and competences. The
EU has a legal personality (Article 47 TEU). Competences are conferred to the
Union, for example in Article 207 TFEU. Therefore, the Union can also
negotiate and conclude agreements with third countries to achieve its
objectives. The Union has finalized agreements not only in CCP, but also in
other fields including the environment.
The EU has taken internal and external measures related to animal
welfare. Those will be discussed below.
5.2. Internal Measures on Animal Welfare
Measures relating to animal welfare include those on the stunning of

animals before slaughter; the protection of animals kept for farming; the
protection for laying hens, pigs, and calves; and animal protection during the
transport30. The EU does not have a specific competence for animal welfare
measures. Therefore, those measures must be incorporated into common
agricultural policies, transport policies, internal market policies, or
environmental policies. Internal measures affect not only domestic industries,
but also third countries, especially those that export goods to EU Member
States. Thus, EU measures have caused conflicts at the WTO level31.
(1) The Ban on Animal Testing for Cosmetic Products

Measures relating to animal testing for cosmetic products affect third
countries including Japan32. Those measures are based on Article 114 TFEU
(formerly Article 95 TEC). Article 114 TFEU forms the legal basis for the
establishment and functioning of the internal market.
Article 7 paragraph 2 Directive 76/768, according to Council Directive
93/35, specifies that an experiment shall not be performed if another
scientifically satisfactory method of obtaining the desired result that does not
entail the use of an animal is reasonably and practicably available33. In 2003,
Directive 2003/15/EC amended Directive 76/768 again 34 . Article 4a of
Directive 76/768 established that Member States shall prohibit “(a) the
marketing of cosmetic products where the final formulation, in order to meet
the requirements of this Directive, has been the subject of animal testing using
a method other than an alternative method after such alternative method has
been validated and adopted at Community level with due regard to the
development of validation within the OECD…(d) the performance on their
territory of animal testing of ingredients or combinations of ingredients.”
Directive 2003/15/EC was replaced by Regulation 1223/2009. Regulation
30
Nakanishi, Y. (2016), pp.88-91.
31
Perišin, T. (2015), “EU Regulatory Policy and World Trade,” European Constitutional Law
Review, 11, pp. 99-120.
32
Nakanishi, Y. (2016), pp.101-104.
33
Council Directive 93/35 of 14 June 1993 amending for the sixth time Directive 76/768/EEC on
the approximation of the laws of the Member States relating to cosmetic products, OJ 1993
L151/32.
34
Directive 2003/15 of the European Parliament and of the Council of 27 February 2003
amending Council Directive 76/768/EEC on the approximation of the laws of the Member
States relating to cosmetic products, OJ 2003 L66/26.
1223/2009 repealed and replaced Directive 76/76835. Regulations are stronger

than directives, strengthening the measures for animal testing. Article 18
paragraph 2 of the Regulation specifies that the period for implementing bans
on the sale of cosmetic products and animal testing ends on March 11, 2013,
and the period for implementation of tests concerning repeated-dose toxicity,
reproductive toxicity and toxicokinetics shall be limited March 11 2013. The
2009 testing ban, 2009 marketing ban, and 2013 marketing ban were overseen
by the EU institutions. Japanese cosmetic products companies such as
Shiseido, Mandom, Pola, and Menard announced they would stop animal
testing of their products. Thus, Japanese companies, along with those of other
countries that export cosmetic products to Member States of the EU, are
obliged to comply with the measures for their products to be marketed in the
EU.
(2) The Trade in Seal Products

Another example is regulation 1007/2209 on trade in seal products 36 .
Regulation 1007/2009 concerning trade in seal products was adopted by the
European Parliament and the Council on 16 September 200937. Its legal basis is
Article 95 TEC (now Article 114 TFEU), whose preamble (1) states that seals
are sentient beings that can experience pain, distress, fear, and other forms of
suffering. Paragraph (13) of the Regulation establishes that related rules
should apply not only to seal products originating in the Community (now
Union), but also to those introduced into the Community (now Union) from
third countries. According to Article 3 of the regulation, “the placing on the
market of seal products shall be allowed only where the seal products result
from hunts traditionally conducted by Inuit and other indigenous communities
and contribute to their subsistence.” After this regulation, in fact, third
countries, especially Canada and Norway, were able to export seal products to
Member States of the EU.
Canada and Norway challenged Regulation 1007/2009 and the
implementation of Regulation 737/2000 under the WTO Agreement on
Technical Barriers to Trade (TBT Agreement), especially Article 2.1 and 2.2
of the TBT Agreement and the General Agreement on Tariffs and Trade
(GATT). The Panel was in favor of the EU and agreed that the ban pursued a
35
Regulation 1223/2009 of the European Parliament and of the Council of 30 November 2009 on
cosmetic products, OJ 2009 L342/59.
36
Nakanishi, Y.(2016), pp. 109-111.
37
Regulation 1007/2009 of the European Parliament and of the Council of 16 September 2009 on
trade in seal products, OJ 2009 L286/36.
legitimate objective (public moral concern about seal welfare) 38 . Although

Canada and Norway appealed to the Appellate Body, it upheld that the EU seal
regime was necessary for public morals as defined by Article XX (a) of the
GATT 194739. This meant that the ban on seal imports by the EU was justified,
based on public morals 40 . The EU measures have thus affected the third
countries and the consideration of animal welfare has become and will remain
globally meaningful.
(3) Short Summary

There is no specific legal basis for animal welfare, but measures that pay
attention to animal welfare can be adopted based on several legal bases such as
Article 114 TFEU.
Even the Union’s internal measures affect third countries because
companies and others export products to EU Member States. They cannot
export goods unless the goods comply with the EU rules. The concept of
animal welfare thus spread the EU measures around the world.
5.3. External Measures for Animal Welfare
(1) FTAs
The Union can negotiate and conclude agreements with third countries
and international organizations. The EU has concluded and is negotiating Free
Trade Agreements (FTAs) with third countries. For example, the EU and
South Korea concluded a FTA, which has already entered into force. The
Union is negotiating a Transatlantic Trade and Investment Agreement (TTIP)
with the USA. The Union finalized negotiations of the Comprehensive
Economic and Trade Agreement (CETA) with Canada. The EU and Singapore
concluded a FTA on October 17, 2014, although it has not yet been approved
formally by the EU41. The negotiations of a FTA between the EU and Vietnam
were completed on 2 December 2015. The EU and Japan are also negotiating a
FTA.
38
WT/DS400/R, WT/DS401/R.
39
WT/DS400/AB/R, WT/DS401/AB/R.
40
Cf. Serpin, P. (2016), “The Public Morals exception after the WTO Seal Products Dispute: Has
the Exception Swallowed the Rules,” Columbia Business Law, Review, p. 217; Levy, P.I. &
Regan, D.H. (2015),“EC-Seal Products: Seals and Sensibilities,” World Trade Review, 14, pp.
337-379; Krämer, L. (2015), p. 422.
41
The case of draft agreement between the EU and Singapore is pending before the Court of
Justice of the EU (Opinion 2/15, OJ of the EU 2015 C363/18).
The main subject matter of those FTAs is trade. However, they are not
simply trade agreements and sustainable development is covered in their
chapters42. For example, Chapter 13 of the FTA between the EU and Singapore
covers trade and sustainable development. Some texts and draft texts of FTAs
that have been negotiated are available online, so provisions related to animal
welfare will be discussed in the following section.
(2) Animal Welfare in the FTAs
① The FTA between the EU and South Korea

The EU and South Korea began to negotiate a FTA in 2007, and
concluded it on 15 October 200943. It entered into force on 1 July 2011. It
comprised a political agreement and a Framework agreement, both of which
established policies on environmental issues44.
For instance Chapter 5 of the FTA between the EU and South Korea is
entitled “Sanitary and phytosanitary measures.” Article 5.1 paragraph 2 of this
chapter states “this Chapter aims to enhance cooperation between the Parties
on animal welfare issues, taking into consideration various factors such as the
livestock industry conditions of the Parties.” Article 5.9, “Cooperation on
animal welfare” states that “the Parties shall (a) exchange information,
expertise, and experiences in the field of animal welfare and adopt a working
plan for such activities, and (b) cooperate in the development of animal
welfare standards in international fora, in particular with respect to the
stunning and slaughter of animals.”
② The CETA between the EU and Canada

The EU and Canada finished negotiations in August 2014. The
Commission adopted a text of the agreement (CETA) in July 2016; it has not
yet been finalized by the Council.
The EU and Canada had a conflict over the trade in seal product in the
WTO, as previously noted. Chapter 5 of CETA, “Sanitary and phytosanitary
42
Leal-Arcas, R. & Wilmarth, C.M. (2015), “Strengthening sustainable development through
regional trade agreements,” In J. Wouters, A. Marx, D. Geraets, B. Natens, Global
Governance through Trade, Edward Elgar, pp. 92-123.
43
OJ of the EU 2011 L127/1, Council Decision of 16 September 2010 on the signing, on behalf
of the European Union, and provisional application of the Free Trade Agreement between the
European Union and its Member States, of the one part, and the Republic of Korea of the other
part.
44
Durán, G.M. & Mogera, E. (2012), Environmental Integration in the EU’s External Relations,
Hart Publishing, pp, 117-127.
measures,” refers to animal health, but makes no references to animal welfare.

For example, Article 5.2, “Objectives” states that the objectives of the chapter
are to (a) protect human, animal, and plant life or health while facilitating
trade, (b) ensure the Parties’ sanitary and phytosanitary (“SPS”) measures do
not create unjustified barriers to trade, and (c) further the implementation of
the SPS Agreement. This differs from the FTA between the EU and South
Korea.
On the other hand, the term “animal welfare” does appear in Article 21.4
of Chapter 21, “regulatory cooperation.” Article 21.4 (s) states that the Parties
endeavor to fulfill the objectives set out in Article 21.3 by undertaking
regulatory cooperation activities that may include “(s) exchanging
information, expertise, and experience in the field of animal welfare in order to
promote collaboration on animal welfare between the Parties.”
③ The FTA between the EU and Singapore

The EU and Singapore finished negotiations for a comprehensive free
trade agreement on 17 October 201445, although it has not yet been concluded.
Annex 5-A of Chapter 5 of the draft of the FTA is “Sanitary and
phytosanitary measures.” “Competent Authorities” of the Chapter refers to
animal welfare. Article 1 of Annex 5-A states that “the competent authorities
of the Union include Member States’ administrations and the European
Commission. In this respect, the following applies: (a) as regards exports to
Singapore, the Member States’ administrations are responsible for control of
the production circumstances and requirements, including statutory inspections
and issuing health (or animal welfare) certifications attesting to the agreed
standards and requirements.” Annex 5-B establishes requirements and
provisions for the approval of establishments for products of animal origin.
④ The FTA between the EU and Vietnam

The EU and Vietnam finished negotiations for an FTA in December 2015.
Its draft text is available, but the numbering of the draft text of the FTA is
incomplete.
Chapter 7 of the FTA is “Sanitary and Phytosanitary Measures.” The
objectives of the Chapter are to protect human, animal, or plant life or health
in the territory of each Party while facilitating trade between the Parties and
ensuring that SPS measures imposed by each Party do not create unnecessary
obstacles to trade. Paragraph 2 of its general provisions states that “each Party
45
http://trade.ec.europa.eu/doclib/press/index.cfm?id=961.
commits to apply the principles of the SPS Agreement in the development,

application, or recognition of any sanitary or phytosanitary measure with the
intent to facilitate trade among the Parties while the Parties while protecting
human, animal, or plant life or health in the territory of each Party.” Paragraph
1(b)(i) of its article “Competent Authorities and contact points” states that “as
regards exports to Vietnam, the Member States are responsible for the
production circumstances and requirements, including statutory inspections
and issuing health and animal welfare certifications attesting to the agreed
standards and requirements.” A “General exception” of Chapter 8, “Trade in
Services, Investment, and E-commerce” cites the goal to “protect to human,
animal, or plant life or health.” Article 6 of the chapter “Trade and Sustainable
Development” refers to enhancing cooperation, as appropriate, to propose new
animal and plant species for amendments to appendices I and II to the
Convention on International Trade in Endangered Species of Wild Fauna and
Flora (CITES).
⑤ The TTIP
The EU and the USA are negotiating the TTIP. Some related documents
have been made public. The Commission published a proposal regarding
sanitary and phytosanitary measures (SPS)46.
Article 1 “Scope and coverage” states that the chapter shall also apply to
collaboration on animal welfare matters. Article 2, “Objectives” states that the
objectives of the chapter are (1) to facilitate trade between the Parties to the
greatest extent possible while preserving each Party’s right to protect human,
animal, or plant life and health in its territory while respecting each Party’s
regulatory systems, risk assessment, risk management, and policy
development process and (2) to provide a framework for dialogue and
cooperation with a view to enhancing the protection and welfare of animals
and reaching a common understanding about animal welfare standards. Article
10 is related to animals, animal products, and animal by-products. Article 17
explicitly covers animal welfare and mandates the following:
“1. The Parties recognize that animals are sentient beings. They undertake
to respect conditions for live animals and animal products that are aimed to
protect their welfare.
2. The Parties undertake to exchange information, expertise, and
experiences in the field of animal welfare with the aim to align regulatory
46
http://trade.ec.europa.eu/doclib/docs/2015/january/tradoc_153026.pdf.
standards related to breeding, holding, handling, transportation, and slaughter

of farm animals.
3. The Parties will strengthen their research collaboration in the area of
animal welfare to develop adequate and science-based animal welfare
standards related to animal breeding and the treatment of animals on the farm
during transport and at slaughter.
4. In accordance with Article 19 [Collaboration in international fora
(multilateral and bilateral)], the Parties undertake to collaborate in
international fora with the aim to promote the further development of good
animal welfare practices and their implementation…”
This is the proposal made by the European Commission before negotiating

with the USA. Therefore, the contents of the proposal directly express the
Union’s will.
(3) Political Agreements

The EU is eager to negotiate and conclude binding political agreements
with concretized political principles, which are now established in Article 21
TEU as previously noted. For example, Japan is negotiating an FTA, but is
also negotiating a political agreement, a so-called strategic partnership
agreement with the Union. This was requested by the Union.
The EU and Vietnam have concluded their FTA. In 2012, the Framework
Agreement on Comprehensive Partnership and Cooperation (PCA) between
the EU and Vietnam was signed47. This was done after the Treaty of Lisbon,
which first ruled on animal welfare.
The PCA clearly refers to animal welfare. Article 14 paragraph 3 of the
PCA, “Sanitary and Phytosanitary and Animal Welfare Issues” states “the
Parties agree to cooperate for animal welfare as necessary, including technical
assistance and capacity building for the development of animal welfare
standards.” Article 32 paragraph 1(e), “Agriculture, Forestry, Livestock,
Fisheries, and Rural Development,” states that the Parties agree to enhance
cooperation, including through strengthened dialogue and the exchange of
experiences with animal welfare.
(4) The Right to Regulate

FTAs recently concluded by the EU include provisions for the right to
regulate. The right to regulate was requested by NGOs and consumers as well
47
http://eeas.europa.eu/delegations/vietnam/documents/eu_vietnam/pca.pdf.
as the EP, who were concerned about lowering levels of protection as a result
of those agreements.
For example, the Commission’s proposal48 for TTIP Article 2 paragraph 1,
“Investment and regulatory measures/objectives,” states that “the provisions of
this section shall not affect the right of the Parties to regulate within their
territories through measures necessary to achieve legitimate policy objectives,
such as the protection of public health, safety, environment, or public morals,
social or consumer protection, or promotion and protection of cultural
diversity.” Animal welfare is not directly mentioned, but related issues such as
the environment and public morals are regulated. Therefore, it might be
possible for the EU to insist on the right to regulate based on its measures for
animal welfare.
(5) Short Summary

The concept of animal welfare appears in the FTAs concluded by the EU
or under negotiation with third countries. After the Treaty of Lisbon in
particular, the concept of animal welfare came to be introduced into the
Union’s external relationships. Draft texts have been written through
negotiations between the EU and third countries. An important example is the
Commission’s proposal for the TTIP. The concept of animal welfare is not
seen only in the FTAs, but also in political agreements.
CONCLUSION
The introduction of the concept of animal welfare into the EU meant the
evolution of the Union’s ethic from anthropocentrism to a higher level of
concern for animal suffering. Initially, the aim of the Community (now the
Union) was economic integration. However, its aims came to include
integration in non-economic areas such as the environment and sustainable
development. The Treaty of Lisbon established a provision for animal welfare
in the TEU for the first time.
After the Treaty of Lisbon, the EU had own values. The EU applies
political principles consistent with its values to its relationships with third
countries.
The Union has taken measures to promote animal welfare. Those
measures were motivated by public entities such as NGOs, consumers, and the
48
http://trade.ec.europa.eu/doclib/docs/2015/november/tradoc_153955.pdf.
EP. The Union’s internal measures affect third countries whose companies
export products to EU Member States because they are obliged to comply with
the Union’s standards. This represents the application of internal measures to
the external field. On the other hand, the concept of animal welfare is also seen
directly in the Union’s external actions such FTAs with third countries. Such
measures lead to the globalization of the Union’s values.
The author would like to thank Enago (www.enago.jp) for the English
language review. This work was supported by JSPS Grands-in-Aid for
Scientific Research (KEKENHI) for 2016.
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BIOGRAPHICAL SKETCH
Yumiko Nakanishi
Affiliation:
Professor of European Union Law at Graduate School of Law,
Hitotsubashi University, Tokyo Japan (since April 2012). Director of the EU
Studies Institute in Tokyo (EUSI), Member of the Board of Directors of the
European Union Studies Association-Japan, Representative of the Hitotsubashi
Association of European Union Law, Member of Japan Association of
Environmental Law and Policy, Member of Japanese Society of International
Law, Member of the Japanese Association of World Law, Member of
Forschungsgesellschaft für deutsches Verfassungsrecht, Japan. Her fields of
resarch are Competence issues in the EU, EU constitutional law, EU
environmental law and EU external relations law.
Education:
1987-1991 Osaka University, 1991 Bachelor of arts, 1991-2000 Legal
Studies at Universities of Hitotsubashi and Münster, Germany. 1993 Master of
Law (Hitotsubashi University), 1995 Master of Law (University of Münster),
1998 Doctor of law (University of Münster).
Research and Professional Experience:

2000-2002 Lecturer of European Union Law, Senshu University, Tokyo,
2002-2008 Associate Professor of European Union Law, Senshu University,
2008-2012 Professor of European Union Law, Senshu Univeristy.
Publication Last 3 Years:
(Books)
Yumiko Nakanishi (ed.), Contemporary Issues in Environmental Law –
the EU and Japan-, Springer 2016; Collection of Case law Analysis regarding
EU competences, Shinzansha, Tokyo 2015 (in Japanese) pp. 1-574, Legal
structure of EU competences, Shinzansha, Tokyo 2013 (in Japanese), pp. 1-
406; European Union Law, Shinseisha, Tokyo 2012 (in Japanese), pp. 1-357;
(Articles in Books)
“Introduction: The Impact of the International and European
Environmental Law on Japanese Basic Environmental Law” and “The
Principle of Animal Welfare in the EU and Its Influence in Japan and the
World,” in Yumiko Nakanishi (ed.), Contemporary Issues in Environmental
Law, Tokyo, Japan, Springer, pp. 87-113; “Legal measures toward Euro Zone
Crisis” in Eiji Ogawa (ed.), The Euro Zone Crisis and the World Economy,
University of Tokyo Press, 2015, pp. 69-106; “Development of political
principles in external action of the EU,” in Noriko Yasue (ed.), The EU and
global governance, Horitsubunkasha, Kyoto, 2013, pp. 69-100;
(Articles in Journals)
“Economic Partnership Agreement between Japan and the European
Union and Legal Issues－A Focus on Investment－,” Hitotsubashi Journal of
Law and politics, Vo. 44, pp. 19-30, 2016; “Development of EU Exclusive
Competences for the Conservation of Marine Biological Resources” The
Hitotsubashi Journal of Law and International Studies, Vol. 13 No.2, 2014,
pp. 53-91 (in Japanese); “Political Principles in Article 21 TEU and
Constitutionalism,” Hitotsubashi Journal of Law and Politics, Vol. 42, 2014,
pp. 11-23 (in English).
Research for Preliminary ruling of the EU’ appear bimonthly in

Jichikenkyu since September 2009 until now continue (in Japanese).
Chapter 5
MOVING IN THE RIGHT DIRECTION:

PAINFUL HUSBANDRY PROCEDURES TEND
TO BE A THING OF THE PAST
Agustín Orihuela *
Faculty of Agricultural Sciences,

Universidad Autónoma del Estado de Morelos,
Cuernavaca, Morelos, México
ABSTRACT
Early painful husbandry practices that were standard procedures in
animal production some years ago, have almost become obsolet.
Examples of these practices include: the trimming of beaks, toes, combs
or wattlers and the production of capons on birds; penis deviation,
reduction of the preputial orifice, blocking of the sigmoidal flexure,
electroeyaculation and dehorning on ruminants; the use of nose rings and
sugical castration on pigs; branding and lip tattoo on horses and mulesing
on sheep.
Most of these procedures have been substituted for more eficient and
painless alternatives. In addition, for those painful procedures that
continue to be applied, several pain control protocols have been
developed based on the use of different combinations of sedatives,
anestethics and analgesics, particularly using the last generation of
nonsteroidal anti-inflammatory drugs to minimize pain when animals are
*
Corresponding Author Email: aorihuela@uaem.mx.
148 Agustín Orihuela
subjected to such practices. It can not be denied the importance that a

more participative society involved in how farm animals are raised, a
growing demand for healthier animal products and the cummulative
scientific results of a developing animal welfare sciene have had in the
significant improvement of the animal wellbeing.
Keywords: welfare, wellbeing, practices, farm, production
INTRODUCTION
Several decades ago, farm animals were subjected to many different
painful procedures, which have gradually disappeared or being replaced by
more modern and efficient procedures.
Some of these procedures used in the past were for example:
Toe trimming in birds, a painful procedure which even though nowadays
is still applied in some turkeys, is not used in the broiler industry any more
(Hester, 2005). Beak, comb and wratlers trimming was another common
practice in many bird species (Gustafson et al., 2007) as well as beak
trimming. Today, due to public opposition to battery cage confinement, many
egg producers are switching to cage-free, organic or range-free systems.
Unlike battery hens, in the later systems hens are able to walk, spread their
wings and lay their eggs in nests, significantly improving the level of animal
welfare than do battery cage systems. Furthermore, due to the lighter density,
enriched nutrition and environment, and exercise, less hens have part of their
beaks burned off as a cannibalism control. In addition, new techniques like the
use of infrared light for beak trimming seems to induce less deleterious
conditions in chickens (Dennis et al., 2009), while the use of genetic lines of
hens with a low rate of cannibaism are becoming more popular
(Craig & Muir, 1993).
The development of controlled methods of reproduction where only one
male is used in a pen of hens, and the advance of new cage designs, have
favored the vanish of procedures like trimming of combs and wattles, justified
earlier by the lesions produced by the fighting between rosters and the trapping
of large combs of certain lying hens lines in older facilities
(Hester et al., 2015), respectively.
Similarly, the production of capons (chickens without their testicles) that
was developed to satisfied a very specific meat characteristics market demand,
no longer exists (Echarri, 1952).
Moving in the Right Direction 149
Furthermore, the development of less aggressive lines of hens in the egg

production industry has reduced beak trimming in these animals (Millman &
Duncan, 2000).
On the other hand, male ruminants in the early days of controlled animal
reproduction, when artificial insemination (AI) was spreading, were subjected
to mayor surgical procedures to provide the industry with bulls, bucks and
rams that will detect females in estrus while avoiding undesired pregnancies.
Procedures like the deviation of the penis, reduction of the preputial orifice
and blocking the sigmoidal flexure were common in order to avoid copulation
(National Agricultural Institute, 2015). Nowadays none of these practices are
used any more, and AI is conducted at fixed time after ovulation induction and
estrous synchronization, or androgenized cows might be used as heat
detectors. In the future, electronic devices will become more generalized,
where cows are individually monitored using telemetric devices that measure
locomotor activity, body temperature, food consumption, milk production,
mounting activity or other parameters that are used to determine the time of
ovulation.
Electroejaculation was another painful procedure (Stafford et al., 1996;
Orihuela et al., 2009 a, b). This practice has been banned in several countries,
and where still in use, it is recommended that animals should be subjected to
general anesthesia before being expose to this semen collection method
(Damián y Ungerfeld, 2011). In the near future, electroeyaculation might be
replaced by transrectal ultrasonic-guided massage, which appear to be a better
option for the same porpose, while avoiding or reducing to a minimum the use
of electricity as stimulus (Ungerfeld et al., 2015, 2016).
Similarly, dehorning on beef cattle is gradually shifting toward beef
production based in genetically poled breeds.
On pigs, the insertion of rings in the nose was another painful procedure
that has become less and less used. When this practice started, rings or wires
were inserted through the septum of the nose to reduce digging in sows on
pasture (Studnitz et al., 2007), later on, clips substituted the rings, and are now
clipped to the rim of the nose, not through the nostrils, and instead of several
rings, the use of only one ring is promoted in order to allow certain digging in
the sows while in pasture.
Surgical castration is another example of standard procedures in the pig
industry that was generally applied without any pain control protocol in young
animals, to avoid the flavour of the meat (Sutherland et al., 2012) from entire
adult pigs. Today, a more conscious society demands for leaner meat and a
more ethic treatment to animals, resulting in a decrease in the use of this
procedure, which is today banned in the organic production systems and in

some countries, like Ireland (Fredriksen et al., 2009). Furthermore, this
procedure is falling into desuse, and new painless alternatives are increasing in
popularity. Surgical castration is now being substituted by procedures like
immunocastration, and today, several commercial vaccines are available in the
market for cattle, pigs and sheep. Inmunological procedures, or the production
of intact males slaughtered before reaching sexual maturity, are alternative
options with increasing producers acceptance. In the future, spermatic
selection, which is now a technology under research, will allow breeders to AI
sows with xx spermatozoa to produce only female offspring, avoiding the
production of males for fattening, and the alleged need to castrate them.
On horses and other species, many countries have banned painful
identification procedures including hot or cold branding and tattoos. Modern
husbandry is moving to radiotransmission devices which are used more and
more every day. Different kind of radiotransmission devices are now available
in the market, and new designs and methods for their placement in animals,
are still in research (Caja et al., 2004).
Iris scanning, is one of the identification methods that will surely occupy
an important place in the days to come. The iris scan cameras are currently at
several large equine hospitals around the United States and in pilot projects in
Ireland, Denmark and Italy. There is no need to do anything invasive to the
animals, and in contrast with devices like microchips or brandings or tattoos,
no alterations can be made to this system that even works with 60% of the iris
damaged (USDA, 3013).
On sheep, mulesing is another extremely painful procedure which has
been in the scope of the society. Subjected to several boycotts in the textile
industry and a strong pressure from animal welfare groups, Australian
government is now giving signs of intentions to ban this practice. There are
several painless alternatives under research for this procedure, for example: an
antiflies long duration vaccine or the development of genetic programs based
on the selection of animals resistant to fly strokes, with less skin folds on the
affected area. These kind of programs, in association with fly-control
campaigns, offer promising possibilities for success (Phillips, 2009).
The list can go on enumerating other painful procedures which fortunately
are left unused. However, some of them are still in use. Fortunately, nowadays
several pain control protocols have been developed and offer another
alternative based on the use of sedatives, anesthetics and analgesics,
particularly among the later, those known as non-steroidal anti-inflammatory
drugs. The combination of these drugs offer a new option to control the pain
induced by procedures like dehorning.
Contributing to the disappearance of painful practices, many countries are
legislating against these kind of procedures, or enforcing laws that at least
constrain the implementation of such practices to be performed under the
supervision or by a veterinarian, during the early days of life of the animals
and with the use of anesthetics and pain killers.
It looks like modern animal husbandry is moving in the right direction.
The welfare of animals has become an important subject in farm animal
production. A more participative society involved in how productive animals
are raised, and a growing demand for healthier animal products certainly have
favored this situation and contributed to interesting and promising advances in
the development of alternatives to those earlier husbandry painful procedures.
However, many painful procedures are still practiced. Some due to lack of
knowledge of the alternative modern technologies available, tradition, or lack
of interest in animal sentience. The goal would be to replace all painful
procedures with new painless alternatives, using among other strategies: a
greater awareness of the scientific advances and the development of new
technologies; improve laws based on the opinion of scientific experts and
capacitation of the people related to handling of animals.
Without guard down, it seems that we are moving in the right direction.
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inflicted injuries among caged hens. Poultry Sci, 72:411-420.
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electoejaculated rams to electroejaculation: hormonal, physiological,
biochemical, haematological and behavioural parameters. Reprod Dom
Anim, 46:646-650.
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Agricultura. Madrid, España, Julio 1952.
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in Europe. Animal, 3:1480–1487.
Gustafson, L. A., Cheng, H. W., Garner, J. P., Pajor, E. A. & Mench, J. A.
(2007). Effects of bill-trimming Muscovy ducks on behavior, body weight
gain, and bill morphopathology. Appl Anim Behav Sci, 103:59-74.
Hester, P. Y. (2005). Impact of science and management on the welfare of egg
laying strains of hens: A Review. Poultry Sci, 84:687-696.
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Effect of partial comb and wattle trim on pullet behavior and
thermoregulation. Poultry Sci, 94:860-866.
Millman, S. T. & Duncan, I. J. H. (2000). Stain differences in aggressiveness
of male domestic fowl in response to a male model. Appl Anim Behav Sci,
66:217-233.
National Agricultural Institute. Just the facts; Introduction to Animal Science.
2nd ed. Idaho USA, National Agricultural Institute, Inc. 2015.
Orihuela, A., Aguirre, V., Hernández, C., Flores-Pérez, I. & Vázquez, R.
(2009a). Breaking down the effect of electro-ejaculation on the serum
cortisol response, heart and respiratory rates in hair sheep (Ovis aries). J
Anim Vet Adv, 8:1968–1972.
Orihuela, A., Aguirre, V., Hernández, C., Flores-Pérez, I. & Vázquez, R.
(2009b). Effect of anesthesia on welfare aspects of hair sheep (Ovis aries)
during electro-ejaculation. J Anim Vet Adv, 8:305–308.
Phillips, C. J. C. (2009). A review of mulesing and other methods to control
flystrike (Cutaneous myiasis) in sheep. Anim Welfare, 18:113–121.
Stafford, K. J., Spoorenberg, J., West, D. M., Vermunt, J. J., Petrie, N. &
Lawoko, C. R. O. (1996). The effect of electro-ejaculation on aversive
behaviour and plasma cortisol concentration in rams. NZ Vet J, 44:95-98.
Sutherland, M. A., Davis, B. L., Brooks, T. A. & Coetzee, J. F. (2012). The
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anesthesia or analgesia. J Anim Sci, 90:2211-2221.
Ungerfeld, R., López-Sebastián, A., Esteso, M., Pradiee, J., Toledano-Díaz,
A., Castaño, C., Labrador, B. & Santiago-Moreno, J. (2015).
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accessory sex glands in mouflons and bucks. Anim Reprod Sci, Accepted
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iris scan technology for equine identification. (2013-09-02). Available
from: Animal Care Tech Note URL:www.aphis.usda.gov/animal_welfare/
BIOGRAPHICAL SKETCH
Agustín Orihuela
Affiliation: Universidad Autónoma del Estado de Morelos, México

Education: PhD
Research and Professional Experience: More than 30 years in education

and research activities
Publications:
Reyes, V., Orihuela, A.*, Aguirre, V. 2014. A note on the effect of number
(single or twin) and sex of contemporary siblings on male-like play
behavior of lambs (Ovis aries). Journal of Veterinary Behavior, 9: 132-
135.
Orihuela, A.* 2014. Ram`s sexual behavior. Review. Revista Mexicana de
Ciencias Pecuarias, 5: 49-89.
Pérez-Torres, L., Orihuela, A.*, Corro, M., Rubio, I., Cohen, A., Galina, C. S.
2014. Maternal protective behavior of zebu type cattle (Bos indicus) and
its association with temperament. Journal of Animal Science, 92: 4694-
4700.
Hernández, C. E.*, Thierfelder, T., Svennersten-Sjaunja, K., Berg, Ch.,
Orihuela, A., Lidfors, L. 2014. Time lag between peak concentrations of
plasma and salivary cortisol following a stressful procedure in dairy cattle.
Acta Veterinaria Scandinavica, 56: 61-69.
Ungerfeld, R.*, Clemente, N., Bonjour, L., Orihuela, A. 2014. Equine
chorionic gonadotrophin administration to rams improves their
effectiveness to stimulate anoestrous ewes (the “ram effect”). Animal

Reproduction Science, 149: 194-198.
Lacuesta, L.*, Orihuela, A., Ungerfeld, R. 2015. Reproductive development of
male goat kids reared with or without permanent contact with adult
females until 10 months of age. Theriogenology, 83: 139-143.
Vázquez, R., Orihuela, A.*, Flores-Pérez, F. I., Aguirre, V. 2015. Reducing
early maternal licking of male lambs (Ovis aries) does not impair their
sexual behavior in adulthood. Journal of Veterinary Behavior, 10: 78-82.
Maldonado, A., Orihuela, A.*, Aguirre, V., Vázquez, R., Flores-Pérez, I. 2015.
Changes in mother-young relationships with the increasing age of the
lamb in hair sheep (Ovis aries). Journal of Veterinary Behavior, 10:
1-5.
Lakestani, N.*, Aguirre, V., Orihuela, A. 2015. Farm animal welfare and
children: A preliminary study building an attitude scale and educational
intervention. Society and Animals, 23: 363-378.
Freitas-de-Melo, A., Ungerfeld, R., Hòtzel, J., Abud, M. J., Álvarez-Oxiley,
A., Orihuela, A., Damián, J. P., Pérez-Clariget, R. 2015. Mother-young
behaviours at lambing in grazing ewes: effects of lamb sex and food
restriction in pregnancy. Applied Animal Behavior Science, 168: 31-36.
Pérez-Torres, L., Rubio, I., Corro, M., Cohen, A., Orihuela, A.*, Galina, C. S.,
Pablos, J. L. 2015. A pre synchronization program at early postpartum
might increase the chances of Bos indicus cows cycling prior to 50 days
regardless of the length of calf separation. Journal of Reproduction and
Development, 61: 199-203.
Ungerfeld, R.*, Orihuela, A. 2015. Sudden introduction of bucks during the
late luteal phase of isolated does induces a biphasic change in
progesterone concentrations Animal Reproduction, 12: 927-930.
García, J., Orihuela, A.*, Solano, J., Flores-Pérez, F. I., Aguirre, V., Vázquez,
R., Pablos, J. L. 2016. Short-term under-nutrition affects feeding and
sexual behaviour in oestrous-synchronized Saint Croix ewes (Ovis aries).
Journal of Applied Animal Research, 44: 419-423.
Orihuela, A.*, Omaña, J.C., Ungerfeld, R. 2016. Heart rate patterns during
courtship and mating in rams and estrous and non-estrous ewes (Ovis
aries) Journal of Animal Science, 94: 1-7.
Avelar, A., Orihuela, A.*, Vázquez, R., Palma-Irizarry, M. 2016. Maca
(Lepidium meyenii) supplementation increase the sexual capacity of low
but not high sexual performance rams (Ovis aries). Boletín
Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas,
15:12-128.
Orihuela, A., Ungerfeld, R.* 2016. Training rams to court and mate female
goats. Applied Animal Behaviour Science, 176:27-31.
Orihuela, A., Averós, X.*, Solano, J., Clemente, N., Estevez, I. Effect of space
available and previous contact in the social integration of Saint Croix and
Suffolk ewes Journal of Animal Science, 94:1238-1249.
Pérez-Torres, L., Orihuela, A., Corro, M*., Rubio, I., Alonso, M.A., Galina,
C.S. 2016 Effects of separation time on behavioral and physiological
characteristics of Brahman cows and their calves. Applied Animal
Behaviour Science, Accepted for publication.
Orihuela, A.*, Valdez, D., Ungerfeld, R. 2016. The effect of suckling,
permanent or temporal contact with the lamb and contact with males on
the interval lambing–first ovulation in Saint Croix sheep and lamb welfare
at weaning. Applied Animal Behaviour Science, Accepted for publication.
Orihuela, A.*, Clemente, N., Ungerfeld, R. 2016. Close contact with
spontaneously cycling Saint Croix ewes triggers cyclic activity in
seasonally anestrous Suffolk ewes. Animal Production Sci.
INDEX
animal production, x, 78, 147, 151, 155

# animal protection, v, 79, 81, 87, 104, 109,
120, 126, 135
21st century, 63
animal sex tourism, 88, 106, 112, 120
animal sexual abuse, 89, 116
A animal welfare, v, vii, viii, ix, x, xi, 1, 2, 3,
4, 6, 48, 49, 50, 51, 52, 53, 54, 55, 56,
aardvarks, viii, 2, 22, 23, 24, 25, 26, 27, 29, 57, 58, 62, 66, 67, 68, 70, 71, 72, 73, 74,
30, 33, 36, 40, 41, 42, 43, 44, 45, 46, 47, 75, 76, 78, 79, 80, 83, 84, 85, 86, 87, 89,
48, 53, 54 93, 94, 97, 100, 102, 103, 105, 106, 108,
abasement, ix, 87, 104, 116 109, 111, 112, 114, 115, 116, 117, 119,
abuse, x, 88, 89, 90, 108, 116, 117 121, 125, 126, 127, 128, 129, 130, 131,
access, viii, 2, 3, 5, 6, 7, 16, 17, 18, 20, 21, 132, 133, 134, 135, 137, 138, 139, 140,
22, 23, 43, 44, 46, 47, 60 141, 142, 144, 145, 148, 150, 154
acid, 65 animals as property, 105
activity level, 18, 43, 45, 46, 69 anthropocentrism, 129, 142
adaptation, 57, 114 anti-inflammatory drugs, x, 147
Africa, 63, 64, 83, 84 anus, 109, 110, 111
age, 78, 98, 151, 154 anxiety, 10, 15, 18
aggression, 9, 14, 18, 20, 104 appetite, 9, 14, 19
aggressive behavior, 9 aquarium, vii, 2
aggressiveness, 152 Asia, 59, 62, 83
agility, 11 Asian countries, 59
agonist, 52 assault, 90, 91, 92, 112, 113
agriculture, ix, 56, 63, 64, 80, 129 assessment, 3, 8, 11, 12, 14, 20, 49, 50, 51,
Amsterdam Treaty, 57 53, 54
anesthetics, 60, 61, 150, 151 atmosphere, 65
animal behavior, 3, 65 attitudes, ix, 82, 87
animal cruelty, viii, 56, 58, 75, 89, 95, 96, Australasia, 119, 120
98, 99, 100, 101, 111, 112, 115, 119 Austria, 96
animal husbandry, 151 authorities, 76, 77, 78, 101, 112, 134, 139
158 Index
authority, 114
autonomy, 93, 104
C
aversion, 43, 52
campaigns, 150
avian, 50
capacity building, 141
awareness, 78, 131, 151
captivity, vii, ix, 2, 6, 51, 52, 54, 56, 60, 68,
69, 84, 85, 100
B carnivores, 46, 50
case studies, viii, 1
ban, 89, 104, 106, 107, 120, 121, 136, 150 case study, 50, 52, 58, 83
barriers, 22, 23, 24, 29, 33, 34, 36, 37, 38, castration, x, 72, 147, 149, 152
39, 43, 45, 46, 47, 139 cattle, 79, 149, 150, 153
base, 8, 89, 95, 129 causal relationship, 19
basic needs, 2, 69 challenges, viii, 1, 3, 4, 5, 49, 68, 69
bear farming, viii, 56, 60, 61, 75, 82 chemicals, 65
beef, 149 Chicago, 51
behavioral assessment, 19 children, x, 88, 90, 95, 96, 108, 116, 117,
behaviors, vii, 1, 3, 9, 10, 11, 12, 18, 21, 22, 154
23, 24, 26, 28, 29, 30, 33, 34, 36, 37, 39, chimpanzee, 51, 52
43, 44, 47, 50, 51, 57, 69 China, 59, 62, 75, 82, 83
behaviour patterns, vii, x, 88, 97 chinese government, 61
benefits, viii, 1, 21, 67, 72 chinese medicine, 81
bestiality, v, vii, ix, 87, 88, 89, 90, 91, 92, cholecystitis, 62
93, 94, 95, 96, 97, 98, 99, 100, 101, 103, cholelithiasis, 62
104, 105, 106, 107, 108, 109, 110, 111, chronic irritation, 61
112, 113, 114, 115, 116, 117, 118, 119, circus, 60, 102
120, 121 cities, ix, 56, 78
bias, 4, 50, 52, 102 civil liberties, 108
bilateral, 141 civil service, 111
bile, viii, 56, 59, 60, 61, 62, 75, 79, 81, 83, civil society, viii, 55, 57, 79, 130
86 classification, 117
biodiversity, 72, 73, 84, 86 cleaning, 5
biosphere, 65 climate, ix, 56, 75
birds, x, 65, 70, 71, 74, 80, 128, 147, 148 climate change, ix, 56, 75
blood, 4 cloaca, 100
body weight, 152 clothing, x, 88, 89, 94, 102, 116
bone, 72, 81 coefficient of variation, 13, 27
bone growth, 72 coercion, 90
bones, 58 colitis, 19
Brazil, 71 collaboration, 139, 140, 141
breeding, 54, 62, 64, 70, 71, 73, 83, 141 collisions, 65
Britain, 118 color, 11
by-products, 140 commerce, 119, 140
commercial, 26, 72, 74, 132, 150
common agricultural policy, 129
common law, ix, 87, 88, 91, 93, 105, 116
Index 159
common market, 127

common sense, 99
D
communities, 77, 136
daily care, 18
community, vii, viii, 2, 3, 49, 67, 94, 130
danger, 60
compensation, 77
data collection, 6, 8, 11, 47, 49
competition, 10, 63, 64, 121
death penalty, 107
complexity, 3, 5, 21, 51, 79
deaths, 63, 65
compliance, 72, 115, 134
degradation, 63, 95, 116
conditioning, 69
democracy, 126, 130, 133
confinement, 68, 70, 75, 148
Denmark, 88, 89, 103, 106, 107, 112, 116,
conflict, x, 10, 65, 83, 125, 138
120, 121, 150
consent, 89, 90, 93, 94, 102, 103, 116, 132
Department of Agriculture, 153
conservation, vii, viii, ix, 54, 56, 58, 62, 64,
destruction, 63, 81
67, 68, 82, 84, 128
detoxification, 59
conservational parks, ix, 56
developed countries, 70, 71, 75, 78
constitutional law, 144
developing countries, 65, 66, 70, 71, 72, 73,
consulting, 8, 82
74, 77, 78
consumer protection, 142
deviation, x, 90, 147, 149
consumers, 70, 75, 76, 131, 141, 142
diabetes, 5, 19
consumption, 77, 78, 149
diarrhea, 11, 19, 53
contamination, 65
diet, 7, 9, 78, 97
controversial, 67
directives, 128, 134, 136
conversion rate, 72
discomfort, 11, 57
conviction, 91, 112
diseases, 62, 65, 66, 67, 69, 71, 73, 78, 104
cooperation, 8, 14, 133, 138, 139, 140, 141
disgust, 97, 98, 99, 116
copulation, 149
displacement, 13, 27
correlation coefficient, 11
distress, 57, 60, 62, 64, 65, 66, 68, 97, 102,
correlation(s), 11, 13, 18, 19, 21, 28
105, 131, 136
cortisol, 12, 21, 26, 53, 152, 153
distribution, 27, 28, 66
cosmetic(s), 106, 126, 135, 136
DNA, 114
cost, 4, 98
dogs, 65, 66, 82, 100, 101, 117
Council of Europe, 98
DOI, 81, 119, 122
counterbalance, ix, 56
dominance, 10
courtship, 154
donations, 76
crimes, 91, 92, 94, 95, 107
donors, 76
crops, 63, 77
doping, 122
cruelty, vii, viii, 56, 57, 58, 75, 79, 85, 94,
drill monkeys, viii, 2
97, 99, 100, 101, 102, 105, 111, 113,
drug testing, 121
116, 128
drugs, 151
cultivation, 64
cultural heritage, 58
cure, 59 E
cycling, 154, 155
East Asia, 62, 82
ecology, 44, 54
160 Index
economic development, ix, 56, 57, 79 European Parliament, 71, 81, 128, 131, 132,
economic integration, 126, 127, 129, 142 133, 135, 136
economic union, 129 European Union, v, vii, x, 57, 70, 71, 73,
economics, 122 81, 88, 89, 113, 114, 121, 125, 126, 129,
ecosystem, 62, 63 131, 138, 143, 144, 145
education, viii, ix, 50, 55, 56, 57, 67, 79, evidence, 9, 11, 47, 48, 49, 52, 88, 96, 104,
153 106, 108, 109, 129, 131
egg, 100, 148, 149, 152 evolution, 142
ejaculation, 92, 100, 113, 152 excretion, 7, 13, 27
electricity, 149 execution, ix, 87
elephants, 51 exercise, 148
emotion, 52, 90, 102 expertise, 138, 139, 140
emotional experience, 4 exporters, 71
emotional state, 4, 21 exports, 128, 139, 140
endangered, ix, 56, 62, 70, 75, 128 exposure, 69, 111
endangered species, ix, 56, 62, 75, 128 external relations, vii, x, 125, 142, 144
endocrine, 52 extinction, ix, 56, 82
endocrinology, 2, 3, 12, 26, 49 extraction, 12, 26, 59, 60, 61, 62, 75, 79, 83
enforcement, 101 extracts, 13, 27
England, 89, 92, 97, 106, 107, 112, 113,
116, 120
England and Wales, 89, 92, 97, 106, 107, F
112, 113, 116
factor analysis, 53
environmental awareness, ix, 56
farm animals, ix, xi, 50, 56, 70, 76, 141, 148
environmental conditions, 57, 72, 74
farmers, 73, 102
environmental issues, 67, 138
farms, 57, 59, 60, 62, 66, 72, 73, 74, 75, 78,
environmental policy, 127, 128, 129
80, 83, 109
environmental protection, 127
fat, 80
environmental stimuli, 9
fauna, ix, 56, 63, 128
environmental variables, 23
feces, 13, 15, 18, 19, 27, 40, 51
environment(s), viii, 1, 3, 10, 21, 23, 25, 47,
feelings, 52, 97, 99, 104, 116
49, 51, 53, 56, 57, 58, 62, 68, 69, 75, 78,
fever, 59
85, 97, 114, 115, 127, 130, 133, 134,
FGM, 5, 12, 13, 15, 16, 17, 18, 19, 20, 21,
142, 148
26, 27, 28, 40, 41, 42, 43, 46, 47
enzyme, 12, 26
Finland, 88
enzyme immunoassay, 12, 26
fisheries, 129
equality, 126, 133
fishing, 63
equipment, 4
fistulas, 61
ethanol, 12, 26
flavour, 149
ethics, viii, 56, 58, 75, 80, 85, 120
flora, 128
Europe, 73, 127, 128, 131, 144, 152
food, x, 8, 9, 10, 25, 26, 60, 61, 63, 64, 69,
European Commission, 71, 72, 74, 81, 130,
70, 71, 73, 74, 75, 78, 81, 88, 94, 102,
139, 141
149, 154
European Community, 126, 132
food chain, 74, 78
European integration, 126
food production, 71
Index 161
food security, 73, 81

force, 57, 61, 108, 126, 127, 129, 137, 138
H
foreign policy, 133
habitat(s), vii, viii, ix, 1, 2, 3, 5, 6, 7, 8, 12,
forest fire, 63
13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23,
formation, 62, 65
24, 25, 29, 33, 34, 35, 36, 37, 38, 39, 40,
France, 71, 122
41, 42, 43, 44, 45, 46, 47, 48, 51, 56, 62,
free choice, 54
63, 64, 65, 66, 67, 69, 77
free trade, x, 125, 133, 139, 143
hair, 4, 11, 152, 154
Free Trade Agreements (FTAs), x, 125,
hazards, 65, 74
126, 133, 137, 138, 141, 142, 143
healing, 61
freedom, 14, 27, 28, 57, 70, 72, 97, 99, 126
health, ix, 56, 57, 65, 67, 68, 69, 70, 73, 74,
freedom of choice, 99
83, 115, 128, 139, 140
funding, 76
health services, 74
funds, 76
health status, 69
height, 6
G high blood pressure, 59
history, 48, 64, 82
gall bladder, viii, 56, 61, 62, 75 holding spaces, viii, 2, 3
gate way crime, x, 88 homes, 49
gel, 26 homosexuality, ix, 87, 90, 94, 98
General Agreement on Tariffs and Trade Hong Kong, 83, 122
(GATT), 136 hormone(s), 4, 7, 12, 13, 23, 26, 27, 28, 46,
general anesthesia, 149 48, 53
genetic factors, 72 horses, x, 108, 122, 147, 150
genetic programs, 150 host, 99
genetics, 72, 73, 78 house, 85, 108, 109, 118, 119, 120
genitals, 88, 91 housing, vii, viii, 1, 2, 3, 4, 5, 6, 7, 13, 18,
Georgia, 50, 54 19, 20, 21, 24, 27, 28, 29, 30, 33, 34, 35,
Germany, 71, 89, 96, 98, 106, 143, 144 36, 37, 38, 39, 41, 42, 43, 46, 48, 53, 64,
global scale, 76 69, 71, 72
globalization, 143 housing conditions, vii, viii, 1, 5, 6, 13, 18,
glucocorticoid, 5, 12, 17, 18, 20, 26, 28, 41, 19, 20, 27, 28, 39
52 human, viii, ix, 5, 19, 25, 51, 52, 56, 58, 62,
GnRH, 46, 50, 52 63, 64, 65, 66, 67, 68, 73, 77, 78, 79, 82,
gorillas, viii, 2, 5, 6, 7, 8, 12, 13, 14, 15, 16, 83, 85, 89, 90, 94, 95, 96, 97, 98, 102,
18, 19, 20, 21, 48, 53 103, 104, 105, 107, 108, 109, 110, 112,
governance, 130, 145 113, 114, 116, 119, 126, 127, 133, 139,
governments, 131 140
grants, 76, 105 human animal, 51, 90
grazing, 63, 64, 154 human dignity, 126, 133
growth, 72 human health, 65, 73, 78, 127
guidance, 68, 73 human right, 108, 126, 133
guidelines, 51, 68, 70 Hungary, 71, 88
guilt, 108 Hunter, 54
guilty, 92, 112, 113, 115 hunting, 63, 65, 66, 69, 89, 116, 122, 131
162 Index
husbandry, v, x, 5, 8, 9, 10, 12, 14, 147, intercourse, 95, 104, 106, 109, 112, 113,
150, 151 114, 117, 118
hybrid, 71 interface, 82
hypothesis, 96 interference, 98, 116
internal controls, 13, 27
international law, 121, 133
I international relations, 133
international standards, 76
ICC, 12
international trade, 119
ideal(s), 57, 72, 79, 103, 123
intervention, 46, 62, 154
identification, 12, 23, 67, 150, 151, 153
investment, 78
identity, 13, 23, 43, 46, 48
Iowa, 119
idiopathic, 19
Ireland, 87, 88, 89, 92, 93, 98, 104, 105,
idiosyncratic, 9
106, 107, 111, 112, 113, 114, 116, 121,
image(s), 4, 112, 116
122, 150
imagination, 110
iris, 150, 153
Immigration Act, 112
iron, 60
immunocontraception, 66
irritability, 18
impact assessment, 82
irritable bowel syndrome, 19, 52
implants, 24, 46, 47
isolation, 67
imports, x, 125, 128, 137
issues, ix, 3, 4, 56, 62, 63, 68, 69, 70, 76,
imprisonment, viii, 56, 75, 92, 101, 107,
77, 80, 83, 123, 132, 134, 138, 142, 144
109, 111, 112, 113
Italy, 128, 144, 150, 151
improvements, 70
incidence, 73
income, 62 J
indecency, 96
India, 78 Japan, 24, 55, 79, 82, 125, 128, 135, 137,
individuals, viii, 2, 3, 5, 9, 10, 14, 20, 23, 141, 143, 144, 145
26, 44, 48, 62, 66, 67, 68, 77, 101, 104 judiciary, 93
indoor habitat, viii, 2, 5, 6, 7, 12, 13, 14, 15, jumping, 64
16, 17, 18, 19, 20, 21, 23, 24 juries, 92
induction, 149 jurisdiction, 105
industrial chemicals, 65 justification, 105
industries, 135 juveniles, 109
industry, 60, 78, 83, 138, 148, 149, 150
infection, 61
inferences, 4 K
inflammation, 59
keeper ratings, viii, 1, 18, 54
ingredients, 58, 135
Korea, 59, 138
injuries, 64, 65, 66, 72, 97, 102, 151
injury, 57, 60, 90, 93, 97
insertion, 109, 149 L
inspections, 73, 74, 139, 140
institutions, 3, 129, 130, 131, 133, 136 landscapes, 81
integration, 126, 127, 129, 142 Latin America, 63, 83
Index 163
laws, ix, 70, 87, 89, 92, 99, 103, 105, 113, methodology, viii, 2, 48
116, 135, 151 migration, 64, 66
Leahy, 121, 122 migration routes, 64, 66
legal paternalism, 89, 93, 104, 105, 116 Minneapolis, 85
legislation, vii, ix, 75, 87, 89, 93, 94, 95, 96, MMA, 122
101, 102, 103, 104, 105, 106, 107, 108, models, 13, 19, 27, 28, 52
111, 112, 113, 114, 116, 132 morality, 89, 93, 94, 99, 108, 118, 128
lesions, 97, 148 morbidity, 67
liberty, 89, 93, 98, 102, 104, 119 mortality, 61, 67, 81
life expectancy, 81 mortality rate, 61
Likert scale, 8 motivation, 52, 104, 109
litigation, 101 mucosa, 61
liver, 62 mutilation, 108
liver cancer, 62
livestock, 63, 64, 65, 70, 73, 77, 78, 79, 82,
102, 138 N
local conditions, 71, 73
National Research Council, 64, 84
locomotor, 44, 149
natural behaviors, vii, 1, 57, 69
LTD, 85
natural habitats, ix, 56, 68, 128
lying, 8, 60, 148
natural resource exploitation, 63
natural resources, 63, 128, 133
M natural selection, 68
nature conservation, 128
Maastricht Treaty, 129 negative relation, 47
magnitude, 14 neglect, 115
majority, viii, 5, 33, 35, 37, 45, 56, 58, 68, negotiating, x, 125, 137, 140, 141
75, 79, 91, 107 negotiation, 142
mammal(s), 22, 43, 51, 54, 65 Netherlands, 71
management, vii, 1, 5, 47, 49, 51, 54, 62, NGOs, x, 76, 125, 131, 141, 142
63, 65, 66, 67, 77, 78, 86, 133, 152 nitrogen, 12, 26, 65
marketing, 60, 72, 122, 135 nitrogen gas, 12, 26
materials, 4 nocturnal animals, viii, 2, 22
matter, 70, 92, 138 non-steroidal anti-inflammatory drugs, 151
measurements, 19, 50 normal distribution, 13
meat, 71, 73, 74, 77, 78, 81, 82, 89, 116, North America, 51, 52, 80, 85
148, 149 Northern Ireland, 111
media, viii, 55, 57, 79 Norway, 89, 106, 136
medical, 59, 69, 83, 85, 90 novel stimuli, 10
medicine, 58, 59, 62, 68 nutrition, 68, 148, 154
membership dues, 76
mental disorder, 90
mental illness, 115 O
mental impairment, 96
obstacles, 139
mental state, 58
OECD, 135
metabolites, 12, 20, 26, 28, 52
164 Index
offenders, x, 88, 96, 111 piloerection, 10

olfaction, 44 plants, 128
omission, 110 pleasure, 95, 97, 104, 110
operations, 73, 78, 81 poaching, ix, 56, 75
opportunities, vii, 1, 3, 22, 23, 43, 45, 47, polar, 53
68, 130, 131 police, 112
organ, 132 policy, 4, 128, 131, 132, 140, 142
overlap, 42, 57 policy making, 131
overpopulation, 66 politics, 145
ovulation, 149, 155 pollution, ix, 56, 63, 65, 74, 75, 84
polyp(s), 61, 62
population, 64, 66, 67, 74, 77, 78
P population growth, 64
Portugal, 55, 79, 83
pacing, 22, 24, 25, 27, 29, 33, 34, 36, 37,
positive emotions, 50
38, 39, 43, 45, 46, 47, 50
positive reinforcement, 5, 7
pain, x, 57, 59, 60, 61, 62, 64, 66, 68, 75,
poultry, 71, 82
90, 97, 99, 101, 102, 105, 129, 131, 136,
power generation, 65
147, 149, 150, 151
Precautionary Principle, 127
parallel, 13, 27, 77
precipitation, 6
parallelism, 13, 27
predation, 66, 67, 77, 80
paraphilia, 90
predator(s), 64, 65
parasites, 69
prednisone, 12
parents, 23
pregnancy, 154
parliament, 72, 92
preservation, 62
partition, viii, 2
prevention, 53, 57, 97
pasture(s), ix, 56, 63, 64, 149
primary caregivers, 49
paternalism, 89, 93, 104, 105, 116
primate, 8, 11, 18, 49
pathways, 19
principles, 126, 127, 133, 134, 140, 141,
PCA, 141
142, 145
peace, 126
prisons, 95
penis, x, 99, 100, 109, 111, 147, 149
private firms, 74
permit, 88
producers, 71, 73, 100, 148, 150
personal autonomy, 104
product market, 59
personality, 4, 20, 54, 134
production costs, 72
personality dimensions, 20
professionals, 5
personality factors, 20
progesterone, 26, 154
personhood, 96
project, 47, 48
pests, 64, 65
propagation, 59, 66
Philadelphia, 118
property rights, 105
photographs, 91
proposition, 95
physical aggression, 9
protected areas, ix, 56
physical health, viii, 55, 57, 79
protection, ix, 56, 62, 67, 70, 71, 73, 74, 77,
physiology, 50, 68
79, 81, 87, 94, 97, 100, 104, 105, 109,
pigs, x, 66, 71, 72, 73, 74, 78, 81, 135, 147,
149, 152
Index 165
112, 126, 127, 128, 130, 135, 140, 142, reliability, 11, 12, 26
153 religion, ix, 56, 57, 75, 79, 90
proteins, 78 religious terms, ix, 87
psychiatry, 96 reproduction, 70, 104, 148, 149
psychological well-being, viii, 55, 57, 79 repulsion, 92, 131
psychology, 54 requirement(s), 69, 94, 112, 129, 134, 135,
public awareness, 67, 74, 76, 77 139, 140
public concern, 131 researchers, 68
public health, 74, 105, 142 resentment, 98
public interest, 116 reserves, ix, 56, 64, 66
public morals, ix, 87, 94, 137, 142 resistance, 73
public opinion, 130 resources, vii, 2, 3, 10, 43
public policy, 128 respiratory rate, 152
punishment, 93, 94, 107, 109 response, 16, 19, 21, 40, 45, 52, 67, 101,
P-value, 30 106, 110, 152
restrictions, 5, 105, 128
revenue, 60
Q rhino, 59, 81
rights, 66, 80, 95, 102, 103, 105, 119, 121,
quality of life, 54
122, 133
questioning, 110
rings, x, 147, 149
questionnaire, 8
risk, ix, 19, 52, 56, 65, 66, 98, 140
risk assessment, 140
R risk factors, 19
risk management, 140
race, 122 Romania, 88
racing, 121, 122 roots, 61, 95
rape, 92 rotations, 36, 41, 42, 43, 44, 47
rating scale, 8 Royal Society, 85, 112
recognition, 140 rubber, 61
recommendations, 5, 72 rule of law, 126, 133
reconditioning, 69 rules, 57, 71, 74, 130, 136, 137
recovery, 13, 27, 67, 68, 69
recovery process, 68, 69
S
recreational, 114
Red List, 83
sadism, 99
reform, v, 87, 101
safety, viii, 56, 68, 142
regulations, 70, 71, 72, 115, 132, 134
sanctions, 74
regulatory changes, 67
science, vii, viii, 2, 3, 4, 54, 56, 58, 67, 75,
regulatory system, 140
83, 116, 141, 152
rehabilitation, ix, 56, 62, 67, 68, 69, 77, 79,
scientific knowledge, 68, 114
80, 81, 82, 83, 84, 85
scientific method, 48
reinforcement, 67
scope, ix, 56, 70, 79, 110, 150
reintroduction, 70
SEA, 127
relevance, 53
security, 128
166 Index
sedatives, x, 147, 150 South Korea, 137, 138, 139

semen, 103, 114, 149 Spain, 66, 81, 84
sensation, 52 species, ix, 2, 3, 5, 6, 12, 13, 18, 19, 20, 22,
sensitivity, 19, 131 43, 44, 46, 47, 48, 49, 56, 62, 63, 64, 65,
septum, 149 66, 67, 68, 69, 70, 71, 75, 76, 86, 95,
serum, 152 104, 114, 140, 148, 150
services, 63, 82 spending, 6, 8, 10, 18, 43, 48
sex, 44, 50, 88, 89, 90, 92, 93, 97, 99, 103, sperm, 152, 153
104, 106, 107, 108, 109, 111, 112, 114, sphincter, 100
116, 118, 119, 120, 152, 153, 154 squeeze cages, viii, 56, 75
Sex Offenders’ Register, 114 staff members, viii, 2
sexual abuse, vii, x, 88, 89, 90, 96, 97, 101, stakeholders, 77
108, 116, 117 stallion, 103
sexual activity, 111 standard deviation, 15, 16, 17, 40
sexual behavior, 153, 154 starvation, ix, 56, 62, 64, 67, 75
sexual contact, 88, 90, 96, 99, 110 state(s), viii, 2, 25, 45, 51, 55, 57, 88, 82,
sexual desire, 89 89, 94, 97, 98, 104, 108, 114, 128, 130,
sexual intercourse, 89, 91, 95, 106, 107, 133, 136, 138, 139, 140, 141, 142
113, 115, 117 statistics, 14, 29, 83
sexual offences, 96, 107, 112, 116 statutes, 97, 109
sexual offending, 108 steel, 61
sexual orientation, 95 sterilisation, 77
sexual violence, 96, 112 stimulation, 3
sheep, x, 100, 147, 150, 152, 154, 155 stimulus, 149
siblings, 153 stock, 71
signs, 10, 18, 19, 20, 60, 97, 150 stress, 3, 4, 13, 19, 20, 21, 27, 46, 47, 50,
Singapore, 137, 138, 139 52, 53, 68, 71, 73, 78, 84, 151
Single European Act, 127 stress factors, 68
skin, 58, 61, 150 stress response, 21, 46, 47, 53, 151
sociability, 20 structure, 14, 27, 28, 145
social acceptance, 109 subjective well-being, 54
social behavior, 49 sub-Saharan Africa, 22
social environment, 44 subsistence, 136
social group, 64 substrate, 23, 26, 29, 43, 46, 47
social housing, 18 success rate, 77
social influence, ix, 56, 70 succession, 11
social integration, 155 sulfur, 65
social interaction, 25, 45, 46 sulfur dioxide, 65
society, ix, xi, 56, 74, 77, 87, 89, 90, 93, 99, supervision, 151
102, 104, 108, 109, 116, 131, 148, 149, supervisor, 8, 11
150, 151 supplementation, 154
sodomy, ix, 87, 88, 92, 94, 107, 113 Supreme Court, 91, 93
software, 24 surface area, 22
solidarity, 133 survival, ix, 56, 62, 64, 68
solution, 64, 73
Index 167
sustainable development, 76, 127, 133, 138, treatment, viii, ix, 56, 57, 58, 71, 72, 75, 79,
140, 142, 143 83, 88, 96, 100, 101, 102, 105, 106, 115,
Sweden, 89, 106 117, 141, 149, 151
swelling, 59 Treaty of Amsterdam, 129
synchronization, 149, 154 Treaty on the Functioning of the European
Union (TFEU), x, 125, 126, 127, 128,
129, 132, 133, 134, 135, 136, 137
T trial, 91
triggers, 155
Tanzania, 82
tuberculosis, 66
technical assistance, 141
turtle, 59
techniques, 66, 67, 148, 151
technologies, 151
technology, 4, 150, 153 U
teeth, viii, 56, 60, 61
temperament, 153 ultrasound, 152
temperature, 5, 149 underlying mechanisms, 52
temporary housing, 19 United Kingdom, 107, 122
tension, 9, 104 United Nations, 133
territory, 77, 135, 139, 140 United States (USA), 1, 137, 140, 141, 150,
testing, 4, 106, 135 152, 153
testosterone, 46, 53 universality, 133
Thailand, 71 updating, 80
the harm principle, 89, 93, 95, 96, 97, 104, urban, 63, 80, 85
105, 116 urbanization, viii, 55, 64, 79
the offence principle, 89, 93, 98, 99, 116 USDA, 150
thermoregulation, 152
threats, 62, 63, 64
time periods, viii, 2 V
tissue, 61
vaccine, 150
tooth, 61
vagina, 109, 110, 111
tourism, 66, 88, 106, 112, 120
validation, 11, 12, 27, 135
toxicity, 136
vegetables, 60
trade, ix, 56, 58, 63, 71, 82, 106, 126, 129,
victims, 95, 112
131, 133, 136, 138, 139, 140, 142
Vietnam, 79, 137, 139, 140, 141
trade agreement, 138
violence, 95, 96, 104
traditional gender role, 102
vocalizations, 9, 10
training, 5, 7, 8, 9, 10, 12, 14, 68, 78
volunteers, 80
traits, 72
voting, 133
transformation, 28
vulnerability, 64
translocation, 62, 68, 84
transmission, 65, 66
transport, ix, 56, 66, 70, 73, 74, 77, 81, 129, W
135, 141
transportation, 141 waking, 20
Wales, 89, 92, 97, 106, 107, 112, 113, 116
168 Index
Washington, 50, 81, 82, 84 wildlife conservation, 67, 75, 82

waste, 65 wires, 149
water, 25, 60, 61, 63, 64, 65, 69 witnesses, 92
welfare, vii, viii, ix, x, 1, 2, 3, 4, 5, 7, 14, workers, viii, 56, 60, 61
15, 18, 20, 21, 22, 33, 43, 44, 45, 47, 48, working class, 100
49, 50, 52, 53, 54, 55, 56, 57, 58, 62, 63, World Bank, 84
64, 65, 66, 67, 68, 69, 70, 71, 72, 73, 74, World Trade Organization (WTO), x, 125,
75, 76, 77, 78, 79, 80, 81, 82, 83, 84, 88, 126, 135, 136, 137, 138, 143
89, 94, 97, 102, 103, 105, 107, 108, 112, worldwide, 63, 65, 71, 73, 79, 84
115, 116, 117, 121, 125, 126, 128, 129,
130, 132, 134, 135, 137, 138, 139, 140,
141, 142, 143, 148, 151, 152, 153, 155 Z
welfare law, 57, 105
zoo animals, vii, 1, 3, 5, 51
wellbeing, vii, viii, xi, 2, 4, 5, 11, 12, 20, 48,
zoo personnel, viii, 2
50, 53, 126, 148
zoology, 79
white paper, 130
Zoophilia, 88, 89, 90, 93, 102, 116, 117,
wild animals, vii, viii, ix, 56, 58, 62, 63, 64,
118, 120
65, 67, 68, 69, 76, 77, 79, 83
wildlife, ix, 56, 62, 63, 64, 65, 66, 67, 68,
70, 73, 75, 77, 79, 80, 81, 82, 83, 84, 85,
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ANIMAL SCIENCE, ISSUES AND RESEARCH

Additional books in this series can be found on Nova’s website

Additional e-books in this series can be found on Nova’s website

NOTICE TO THE READER

Library of Congress Cataloging-in-Publication Data

ISBN: 978-1-53610-304-5 (e-book)

Published by Nova Science Publishers, Inc. † New York

THE ROLES OF TIME AND SPACE IN

Stephanie M. Allard , PhD, Grace A. Fuller, PhD

and Jennifer L. Hamilton

overnight access to an indoor habitat to more traditional night holding

Keywords: aardvarks, gorillas, drills, animal welfare, zoo, endocrinology

behind-the-scenes holding spaces differ greatly from habitats, both in

indicators of positive welfare, rather than simply focusing on the absence or

These projects, including their methodological challenges and ensuing results,

CASE STUDY 1-GORILLA/DRILL NIGHT HOUSING

The Detroit Zoo is home to three male silverback Western lowland

welfare evaluations (Wemelsfelder et al., 2001). Caretaker ratings of

Subjects and Housing

Night Day Location Keeper Keeper Fecal Fecal

Caretaker Assessments of Behavior

two-week break in data collection during April. Raters were instructed to

Table 2. Final behavior assessment tool for gorillas and drills

4. High: performing high-intensity displays directed towards conspecifics; attempting

Table 3. Inter-rater reliability measures from validation of gorilla-drill

Item ICC ICC Cronbach’s

Hormone Sample Collection and Analysis

cortiscosterone, 0.2% for desoxycorticosterone, and < 0.16% for

Behavior Assessment Data

Biological Validation of FGM Assay for Gorillas

Analysis of FGM by Housing Condition

p = 0.73) or interaction between night and day locations on FGM values

Figure 1. FGM concentrations measured in response to a regularly scheduled

Correlations between Behavior Ratings and FGM Concentrations

As evaluated by keeper ratings of behavior and fecal glucocorticoid

them. Additionally, the drills were perceived to be less aggressive towards

concentrations and behavior, elucidating the interplay between these welfare

CASE STUDY 2-AARDVARKS

Aardvarks (Orycteropus afer) are solitary, nocturnal mammals native to

Table 4 for further details). We developed a study designed to examine if the

Table 4. Description of the three indoor spaces

Housing condition Features

Table 5. Ethogram of aardvark behavior

Videos were coded by four individuals. Inter-observer reliability (IOR >

Hormone Sample Collection and Analysis

The assay was chemically validated for aardvarks by analyzing parallelism

Table 6. Total fecal samples analyzed for fecal glucocorticoid metabolites

Rotation Housing Condition Baji Kaatie Rachaael Roxaane

each individual, descriptive statistics of location and substrate/feature use have

1st Rotation 2nd Rotation

1st Rotation 2nd Rotation

Finally, there was a significant interaction for housing condition and

When examining time by shared barriers, there was no significant effect

condition. In the first rotation, there was no significant difference in amount of

Biological Validation of FGM Assay for Aardvarks

Figure 8. FGM concentrations measured in response to a regularly scheduled

Analysis of FGM by Housing Condition

Figure 9. Fecal glucocorticoid metabolite concentrations (FGM; mean + SE) for

Correlations between Behavior and FGM Concentrations

The aardvarks in this study demonstrated differences in their behaviors

changed. This again suggests a potential influence of neighbor identity on the

Exploration and FGM concentrations did trend towards a negative

The results of these studies highlight the importance of assessing welfare

Fabregas, M.C., Guillen-Salazar, F. & Garces-Narro, C. (2011). Do