Population-Level Risk Factors for Stereotypic Behaviour and Infant Mortality in Captive Carnivores

by Jeanette Kroshko

A Thesis presented to The University of Guelph

In partial fulfilment of requirements for the degree of Master of Science in Animal and Poultry Science

Guelph, Ontario, Canada © Jeanette Kroshko, January, 2015

ABSTRACT

Population-level risk factors for stereotypic behaviour and infant mortality in captive carnivores

Jeanette Kroshko Advisor: University of Guelph, 2015 Professor G. J. Mason

Natural behavioural biology and birth origin were investigated as risk factors for stereotypic behaviour and infant mortality in captive carnivore species. The data for natural behavioural biology, stereotypic behaviour, and captive infant mortality were obtained from literature searches and previously compiled databases. It was found that home-range size, daily distance travelled and chase distance predicted stereotypic behaviour, but not infant mortality. Analyses investigating the interaction between birth origin and natural behavioural biology for stereotypic behaviour were inconclusive due to small sample sizes. In addition, a comprehensive literature review was conducted for birth/hatch origin effects across any/all species. This survey found that captive-born/hatched individuals tended to be more prone to pathologies and wild-caught individuals may have poorer welfare. In conclusion, carnivore species that are wide-ranging or have long chase distances are particularly susceptible to developing stereotypic behaviour in captivity, and birth/hatch origin appears to predict welfare and some forms of pathology.

Acknowledgements

First, I would like to thank my supervisor, Georgia Mason, for all her guidance over the years and for sticking with this project even when it was difficult.

I would also like to thank my collaborators and advisory committee – Ross Clubb, Axel Moehrenschlager, and Tina Widowski – for their support, assistance, and invaluable suggestions. I am also grateful to Axel Moehrenschlager and the Calgary Zoo for kindly allowing me to spend time at the Centre for Conservation and Research.

As well, I am appreciative of Laura Harper and Fernando Salgado-Bierman for assistance with data entry, and all my colleagues at the University of Guelph and the Centre for Conservation and Research for always being there to answer my questions.

I also have to thank NSERC for funding my research.

To my friends, family, and all the people who helped support through the difficult times in so many ways, thank you, I couldn’t have done this without you. I would particularly like to thank Jason Janiak, you made the last year so much easier. A huge thank you to my mom, Joan Krochko, for going above and beyond to help support me in every way possible; words cannot express how grateful I am.

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TABLE OF CONTENTS

List of Tables ...... viii

List of Figures ...... x

Chapter One: General introduction ...... 1

Introduction ...... 1

How and why study captive wild species ...... 4

Welfare...... 4

Species conservation ...... 7

Scientific value of species comparisons ...... 8

Overview of methodologies for species comparisons ...... 8

Comparisons of species welfare in captivity ...... 9

Controlling for phylognetic non-independence ...... 11

Why focus on captive carnivores? ...... 12

Aims of this thesis ...... 13

References ...... 15

Chapter Two: Wild behavioural biology as a risk factor for carnivores in captivity ...... 19

Introduction ...... 19

Methods ...... 23

Updating the captive carnivore stereotypic behaviour database ...... 23

Data collection ...... 23

Quality control ...... 25

Calculation of species medians ...... 27

Updating the captive carnivore infant mortality database ...... 28

Data collection ...... 28

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Quality control ...... 28

Calculation of species medians ...... 33

Updating the wild carnivore behaviour database ...... 34

Data collection ...... 34

Quality control ...... 35

Calculation of species medians ...... 38

Statistical analyses ...... 38

Controlling for confounding factors ...... 38

Running the regression analyses ...... 40

Results ...... 41

Identifying possible confounds ...... 41

Predictors of steretypic behaviour ...... 41

Predictors of infant mortality ...... 44

Discussion ...... 45

References ...... 56

Chapter Three: The effects of birth or hatch origin: how wild versus captive developmental environments can affect phenotype within a single generation ...... 60

Introduction ...... 60

Methods ...... 63

Birth/hatch origin effects ...... 66

Natural behaviour ...... 66

Foraging behaviour ...... 66

Anti-predator behaviour ...... 68

Behaviours related to movement, dispersal, habitat selection ...... 69

Nesting/sheltering behaviour ...... 71

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Self-directed and comfort behaviour ...... 71

Social behaviour ...... 72

Stress and fear in response to anthropogentic stimuli ...... 73

Reproduction ...... 74

Sexual and reproductive development ...... 74

Reproductive behaviour ...... 75

Reproductive disorders and physiology ...... 76

Infant mortality and parental care ...... 77

Offspring differences ...... 79

Overall reproductive output (mechanisms unknown) ...... 79

Physiology and morphology ...... 81

Brain development, behavioural organization, and cognition ...... 82

Abnormal behaviour e.g. stereotypies ...... 83

Morbidity and mortality ...... 86

Health and disease ...... 86

Survival in captivity ...... 87

Survival in the wild ...... 87

Discussion ...... 88

Possible mechanisms underlying birth/hatch origin effects ...... 91

Nutrition in captivity ...... 91

Veterinary care ...... 92

Stress, fear and their functional consquences ...... 93

Environmental complexity and its effects on brain and behavioural

development ...... 96

Physical effects of experience ...... 98

Practicle implications and future research ...... 99

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References ...... 102

Chapter Four: Birth origin as a risk factor for stereotypic behaviour in carnivores ..... 115

Introduction ...... 115

Methods ...... 117

General overview ...... 117

Data collection ...... 117

Quality control ...... 118

Calculation of species medians ...... 118

Confounding factors ...... 119

Statistical analysis ...... 121

Results ...... 122

Discussion ...... 122

References ...... 128

Chapter Five: Final discussion ...... 130

Summary of results ...... 130

Context: a future for wild animals in captivity ...... 133

Future research ...... 135

References ...... 140

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LIST OF TABLES

Chapter Two

Table 1: Species characteristics in the wild and hypotheses and predictions for the development of stereotypic behaviour and increased infant mortality in captivity ...... 24

Table 2: Species listed in the Captive Carnivore Stereotypic Behaviour Databases, the

Captive Carnivore Infant Mortality Databases and the Wild Carnivore Behaviour

Databases ...... 26

Table 3: Species medians for locomotor stereotypic behaviour, all stereotypic behaviour, infant mortality, and wild variables...... 29

Table 4: Sample size for the stereotypic behaviour and infant mortality data ...... 32

Table 5: Journals used for the wild behaviour literature search ...... 35

Table 6: Search terms used to find wild behavioural data for each species ...... 36

Table 7: Relationship between infant developmental rate and infant mortality ...... 41

Table 8: Regression analyses between wild behaviour variables and locomotor stereotypic behaviour, all stereotypic behaviours combined, and infant mortality ...... 46

Table 9: The relationships between home-range size and infant mortality in carnivore databases ...... 47

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Table 10: Relationship between home-range size and infant mortality controlling for reproductive variables ...... 48

Chapter Four

Table 1: Species medians by birth origin ...... 120

Table 2: Interaction between the wild behaviour variables and locomotor stereotypic behaviour and all stereotypic behaviours for birth origin ...... 123

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LIST OF FIGURES

Chapter Two

Figure 1: Relationship between locomotor stereotypic behaviour (% obs) and chase distance (m) ...... 43

Figure 2: Relationship between locomotor stereotypic behaviour (% obs) and home-range size (km2) controlling for body mass (kg) ...... 43

Figure 3: Relationship between locomotor stereotypic behaviour (% obs) and daily distance travelled (km) ...... 44

Chapter Three

Figure 1: Diagram illustrating key definitions and comparisons of captive-bred and wild-bred animals in the wild environment ...... 65

Figure 2: Diagram illustrating key definitions and comparisons of captive-bred and wild-bred animals in the captive environment ...... 65

Chapter Four

Figure 1: Relationship between locomotor stereotypic behaviour (% obs) and home-range size (km2) controlling for body mass (kg) according to birth origin ...... 125

Figure 2: Relationship between locomotor stereotypic behaviour (% obs) and daily distance travelled (km) according to birth origin ...... 125

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Chapter One General Introduction

Introduction

The Order Carnivora consists of a diverse group of 286 species of placental mammals (Nyakatura and Bininda-Emonds, 2012) that are distinguished by scissor-like cheek teeth called carnassials (Nowak, 2005). The species listed in this Order include terrestrial families as diverse as the Felidae (cats), Canidae (wolves, foxes and relatives), Ursidae (bears), and the Pinnipeds, a clade of several families of marine-dwelling mammals such as seals and walruses. The Felidae are the most carnivorous of these families with a diet consisting almost entirely of flesh, while other Carnivora sub-groups vary widely in this regard and include omnivores (e.g. grizzly bears) and plant-eating specialists (e.g. giant panda, Ailuropoda melanoleuca). The term carnivore thus has two meanings in the literature: it is used to indicate a taxonomic grouping, the Order Carnivora, as well as being used as a descriptor for any species with a carnivorous (flesh-containing) diet. Usage of the term ‘carnivore’ in this thesis will always refer to members of the taxonomic grouping of species that form the Order Carnivora.

A large number of wild (non-domesticated) carnivore species and individuals are held in captivity for an array of reasons. For fur production, the most common carnivore species raised in captivity are the mink (Neovison vison), racoon dog (Nyctereutes procyonoides), and red and arctic foxes (Vulpes vulpes, Vulpes lagopus). According to the European Fur Breeders Association 2011 Annual Report (http://www.efba.eu/download/annual_report/2011/index.html) there were more than 52 million mink pelts and 3.7 million fox pelts produced globally in 2011, and 130,000 raccoon dog (Nyctereutes procyonoides) pelts produced in Europe alone. Other carnivore species such as Asiatic black bears (Ursus thibetanus) and tigers (Panthera tigris) are farmed in captivity for organs/tissues to be used in traditional medicines (Nowell, 2010, Graham- Rowe, 2011). For example, tiger bones are used in traditional Chinese medicine and in 2007 there were more than 5000 captive tigers in facilities in China (Nowell, 2010). Ostensibly, those tigers were being bred for reintroduction programs. Bears are farmed for their bile which is used to treat gallstones in traditional medicine (Graham-Rowe, 2011). In 2010 it was estimated that there were 13,000 captive Asiatic black bears (Ursus thibetanus) and Malayan sun bears (Helarctos malayanus) on farms in Asia (Kikuchi, 2012).

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Many species of carnivores are also held in captivity as part of the legal and illegal pet trade. It has been estimated that in the United States alone there may be as many as 12,000 tigers (Nyhus et al., 2003) and 15,000 exotic big cats in total (National Geographic 2009, http://news.nationalgeographic.com/news/2002/08/0816_020816_EXPLcats.html) living in neighbourhoods and roadside zoos. In many jurisdictions it is still legal to acquire and own these large carnivores; however, the costs of maintaining adequate care for these animals is steep, many suffer neglect and eventually these animals end up in sanctuaries or must be destroyed (Nyhus et al., 2003). Captive carnivores (e.g. large cats, bears) are also kept for entertainment purposes in circuses, magic shows (e.g. white tigers at the Mirage Hotel, Las Vegas) and as street performers in various countries (D'Cruze et al., 2011).

There are many large and varied collections of wild animals in zoos globally. Whether these facilities are called zoos, zoological gardens, safari parks, wild life parks or menageries, such collections, even on a minor scale, have existed over centuries originally to display captive wild animals for private and/or public entertainment (Carr and Cohen, 2011). Exotic mammals, and particularly the carnivores, are popular attractions at zoos. Many are top predators that originate from distant continents and provide the viewing public a small glimpse of the biology and landscapes of those unfamiliar regions. Currently, zoos house a diverse array of carnivore species. In 2010, the institutions submitting data to the International Species Inventory System (ISIS) representing more than 800 zoos and aquariums, including 75% of the American Association of Zoos and Aquariums (AZA) and all of the European Association of Zoos and Aquariums (EAZA) members, held more than 125,000 individuals representing all 286 carnivore species (Conde et al., 2011).

Initially, zoos were private facilities and developed as sites of entertainment and displays of power and wealth. Zoological societies formed during the late 18th and early 19th centuries added an emphasis on scientific research and supported the development of truly public zoological gardens (e.g. the London Zoo, 1828). The number of zoos worldwide now exceeds 1,200, and they welcome more than 600 million visitors annually (Carr and Cohen, 2011). These publicly-funded and accessible zoological collections have evolved into cultural and entertaining tourist destinations.

While historically zoos were geared towards public entertainment, it has increasingly been recognized over the last 50 years that their mandate should also include education, and later research and conservation as well. Increasingly, over the past couple of decades, their

2 direction and role has therefore been refocused to reflect concerns over environmental degradation, species extinction, and animal welfare. The World Association of Zoos and Aquariums (WAZA) is the unifying organization for the world zoo and aquarium community with more than 300 member facilities world-wide. WAZA’s Vision for “the full conservation potential of world zoos and aquariums [to be] realized,” reflects the changing roles of zoos and aquariums. Initiatives by zoos that support these visions include: captive breeding programs, such as the Association of Zoos and Aquariums’ Species Survival Plans (www.aza.org/species- survival-plan-program); programs for the reintroduction of endangered species into the wild, such as those for the black-footed ferret (Soorae, Marinari, 2012) and the California condor (Wallace, 2012); solicitation of financial support for in situ conservation efforts (as related to conservation, in situ refers to conservation in a species natural range, while ex situ refers to conservation efforts outside of the natural range); and public education for wildlife conservation and environmental concerns. Zoos are also becoming increasingly concerned about animal care, and this is reflected in WAZA’s commitment to being involved in setting standards for animal welfare, and the Association of Zoos and Aquariums (AZA) Mission Statement that the organization “provides its members the services, high standards and best practices to be leaders and innovators in animal care.” Zoos are becoming more involved in research related to animal welfare, such as studies looking at the effectiveness of environmental enrichment techniques to reduce stereotypic behaviour (Shyne, 2006, Swaisgood and Shepherdson, 2006); where environmental enrichment is defined as a process that seeks to identify and provide environmental stimuli to promote the psychological and physiological well-being of animals (Shepherdson, 1998).

In this chapter I will give an overview of why it is important to study captive wild species for welfare, conservation, legal and scientific reasons; outline the methods we have for doing this, with a special focus on infant mortality and stereotypic behaviour; introduce the idea of variation between species; discuss common methodologies used in species comparisons; and end with a brief overview of the other thesis chapters that follow.

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How and Why Study Captive Wild Species?

The following section is a general outline addressing all wild species in captivity; carnivores will be specifically addressed in more detail later.

Welfare

There is accumulating evidence that animals are sentient beings (Jones, 2013, Proctor, 2012); thus, the provision of inadequate captive habitats leading to poor welfare is no longer ethically responsible. Here welfare refers to the affective state of an individual, thus animals experiencing positive affective states have good welfare, and those experiencing negative effective states have poor welfare (Boissy et al., 2007, Dawkins, 1990, Mason and Mendl, 1993). Welfare can be impacted by factors/experiences such as health, access to food and shelter and the ability to express natural behaviour (Dawkins, 1990, Mason et al., 1998). The large discrepancies between the captive and wild environments, including differences in diet, available space, and social grouping (see Chapter 3) may lead to welfare issues for wild species in captivity. It is not possible to directly measure a state of welfare for animals that cannot communicate easily with us (Mason and Mendl, 1993). Therefore, standardized indicators that have been independently validated are used to infer the welfare state of an individual. These indicators include various aspects of behaviour, disease prevalence, infertility, infant mortality, longevity, and physiological measurements such as stress hormone levels (Fraser, 2008). Infant mortality and stereotypic behaviour are discussed in more detail below since they are the two indicators that this thesis will focus on.

When captive animals are kept under optimal conditions, that allow for normal functioning and behavioural development, their infant mortality should be lower than in the wild due to the removal of predation (Ralls and White, 1995, Steiger et al., 1989, Vanheerden et al., 1995) and provision of adequate resources such as food and shelter (Kauhala and Helle, 1995, Rogers, 1987, Sklepkovych, 1989). However, even under ideal conditions there will always be a certain amount of infant mortality in any population, and thus the presence of infant mortality does not necessarily indicate that there is a problem. This intrinsic level of infant mortality will differ characteristically among species for a variety of reasons; for example, ‘r’ selected species produce more offspring and have higher infant mortality than ‘K’ selected species (Rockwood, 2006). For a discussion of the methods that can be used to determine appropriate baseline

4 levels for traits such as infant mortality and control for the intrinsic inter-species differences see below ‘Comparisons of Species Welfare in Captivity’. When infant mortality levels are higher than expected (after the intrinsic level of infant mortality has been controlled for) it may indicate that optimal conditions are not being provided for the animals (Debyser, 1995, Marker-Kraus, 1997, Promislow and Harvey, 1991). The most prevalent causes of infant mortality across 29 species of captive carnivores involved poor maternal care, and included both infanticide by the dam and maternal neglect (Schmalz-Peixoto, 2003); it was concluded that the infanticide and maternal neglect most likely reflected sub-optimal conditions due to the high prevalence in captivity and that the incidence of infanticide often decreased when individuals were moved to better conditions. These findings suggest conditions of chronic stress, since stress has been shown to impact maternal care in primates and rodents, including the common marmoset (Callithrix jacchus) (Saltzman and Abbott, 2009), gorillas (Gorilla gorilla) (Bahr et al., 1998), and rats (Rattus norvegicus) (Champagne and Meaney, 2006, Patin et al., 2002). Functionally, it is thought that the dams may perceive that the environment is unsatisfactory for reproduction, and this could lead to a decrease in parental investment (Clutton-Brock, 1991) or termination of parental investment (Schino and Troisi, 2005). In some instances, however, inadequate maternal care may reflect abnormalities in the mother; for example, Troisi and D’Amato (1994) found that in a colony of Japanese macaques (Macaca fuscata) bouts of poor maternal care occurred when anxiety was triggered in the mothers and interfered with the complex motor patterns associated with appropriate maternal care. It was noted that these mothers had themselves experienced social deprivation in early development, and the authors thought this was the underlying cause of the anxiety and poor maternal care exhibited in adulthood.

The expression of stereotypic behaviour is associated with conditions that have been independently shown by other indicators to cause poor welfare in captivity (Mason and Latham, 2004). Stereotypic behaviours are defined as repetitive behaviours induced by frustration, repeated attempts to cope, or CNS dysfunctions (Mason and Rushen, 2006), and are prevalent in many captive populations of wild and domesticated species (e.g. elephants, Elephas maximus, Rees, 2009, tigers, Szokalski et al., 2012, mice, Mus musculus, Bechard et al., 2012, pigs, Sus domesticus, Arellano et al., 1992). They are diverse, and include regurgitation and re-ingestion of food, as expressed by apes such as gorillas (Hill, 2009); self-injurious behaviours such as fur-plucking and tail chewing by clouded leopards (Neofelis nebulosa) (Wielebnowski et al., 2002a) and barbering in mice (Garner et al., 2004); and repetitive route-tracing in giraffes

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(Giraffa camelopardalis) (Bashaw et al., 2001), birds (Keiper, 1969), and primates (Pomerantz et al., 2013).

The provision of optimal captive habitats for wild species requires careful research into the requirements for good welfare in a species-specific manner. This is especially important as these requirements may vary widely among species, an issue I return to below in the section on species comparisons. Conducting careful scientific studies on the welfare of wild species in captivity can address the ethical concerns of proper husbandry in captivity and whether certain species should be kept in captivity at all. Although there are processes in place to objectively determine which species to house in captivity, currently, welfare is usually not listed as a criterion used in the decision making process (e.g. Small Carnivore TAG, 2010). In some cases information on the proper care of captive wild species has been used to inform choices about which species to house in captivity and requirements for minimum care standards. For example, the European Association of Zoos and Aquariums (EAZA) Taxon Advisory Groups (TAGS) create Regional Collection Plans to make recommendations on which species should be kept in captivity, and husbandry expertise is one factor taken into consideration. As well, various levels of government have implemented regulations regarding which wild species (including carnivores, reptiles etc.) can be kept in captivity, under what conditions, whether owned by individuals or institutions, and in which jurisdictions, for the protection of handlers, human visitors, the public, as well as for the welfare of the animals themselves (Nyhus et al., 2003). In Canada, federal laws restrict the ownership of endangered species listed by CITES (The United Nations’ Convention on International Trade in Endangered Species of Wild Fauna and Flora; www.cites.org), which is a treaty agreement among governments (179) to ensure that the international trade in wild animals and plants does not threaten their survival. Provincial laws cover other native and exotic wildlife, but these vary across region. Ontario is the only province lacking any form of provincial legislation regarding exotic animal ownership; in Ontario the 2003 Ontario Municipal Act gave municipalities the power to enact exotic animal by-laws, but these are not standardized. Creating these guidelines and regulations can be problematic since there is often a lack of adequate information regarding the specific requirements for particular wild species in captivity (European Commission, 2012). As a result, in general, most exotic wild species do not have species-specific mandatory minimum care standards, and the combination of further research and adequate resources to implement and regulate standards is necessary to ensure good welfare for captive wild animals in Canada and globally.

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Species Conservation

Scientific studies on captive carnivores and other wild animals can also address key issues to improve the contribution of captive populations to species conservation and environmental protection in the wild. Captive breeding programs, such as the AZA Species Survival Plan (SSP) have been instituted to preserve genetic diversity through the establishment of self- sustaining captive populations that do not require supplementation of individuals from the wild. Yet, these programs suffer from founder effects where there is minimal genetic variation as a result of small founder populations (Williams and Hoffman, 2009); inbreeding depression evidenced by reduced fitness from repeated breeding of related individuals (Williams and Hoffman, 2009); adaptation of populations to captivity (Williams and Hoffman, 2009); and breeding problems, such as failure to breed or poor infant survivorship compared to wild populations (Mason, 2010), that contribute to the previously mentioned issues and generally hinder the success of these programs.

Reintroduction programs, which are the ultimate goal for most captive breeding programs (Williams and Hoffman, 2009), may suffer from many difficulties, particularly when captive-born populations are used in the reintroductions (Jule et al., 2008, Harrington et al., 2013). One reason for these failures could be abnormal behaviours (i.e. stereotypic behaviour) and cognitive changes caused by captivity, leading to reduced behavioural flexibility and poor spatial memories (Vickery and Mason, 2003, Campbell et al., 2013). A recent survey of rehabilitation and release practices for mammals did find that stereotypic individuals are commonly released back into the wild (Guy et al., 2013). Stereotypic behaviours may additionally diminish the educational value of the animals, since these activities are not representative of natural behaviours and may be perceived negatively by the public (Swaisgood and Shepherdson, 2006). Miller (2012) investigated this issue and found that members of the public visiting a zoo are less likely to donate money, revisit the zoo, or make positive recommendations about zoos, after observing a tiger engaged in stereotypic behaviour.

Well-designed studies that aim to improve species-conservation efforts can help solve the above mentioned problems. Research has already been used to improve the success rates of captive breeding programs (Wielebnowski et al., 2002b) and reintroduction programs (Shier and Owings, 2006, Reading et al., 2013), to assess the welfare status and the extent of abnormalities present in captive animals (Clubb et al., 2009), and to monitor the effectiveness of public education programs (Price et al., 2009) and ex situ conservation efforts (Fraser, 2008,

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Edwards et al., 2009). In many instances improving the conservation value of a species in captivity goes hand in hand with improving captive welfare, although when individuals habituate to humans in captivitymor for practices such as anti-predator training in preparation for reintroduction (Harrington et al., 2013), this may not be the case.

Scientific Value of Species Comparisons

There is a diverse range in the responses of different species to captivity, with some species seeming to thrive, breeding well and living long lives, while others suffer from numerous behavioural, breeding, and health-related issues (Mason, 2010). By studying these different responses to captivity across species, rather than just the response of one species, it is possible to gain broader insights into welfare and other issues to create a theoretical framework that is applicable to a wide range of species; thus allowing hypotheses that would otherwise be very hard to investigate, such as the importance to welfare of being able to hunt (Mason, 2010), to be tested. This comparative approach is also a valuable opportunity to investigate more fundamental biological questions regarding species differences, such as the diversity of control mechanisms underlying behaviour, the influence of developmental environments, and the evolutionary function of feelings (see below for examples) (Mason, 2010). The first successful example of using comparative approaches to investigate welfare problems was conducted by Clubb and Mason (2003, 2007) on carnivores where home-range size was found to be a risk factor for both stereotypic behaviour and infant mortality in captivity. More recent ones include investigations into factors predicting longevity in captive ruminants (Mueller et al., 2011; see below for details), and factors predicting stereotypic behaviours across the Primates (Pomerantz et al., 2013; see Chapter 2 for details). These approaches are discussed in more detail below.

Overview of Methodologies for Species Comparisons

Comparative methods have been developed to use existing variation between populations or species to address key hypotheses. This type of cross-species analysis can generate broad principles and has predictive power that can be applied to unstudied species (Felsenstein, 1985). However, simple, direct comparisons among species may not always be appropriate

8 due to innate differences in such areas as life history strategies, behaviour and physiology, and this is particularly relevant when comparing species-specific reactions to captivity. Underlying similarities due to the degree of phylogenetic relatedness among species can also confound or mask relationships between the variables studied (Felsenstein, 1985). Thus, careful thought and planning, and specific statistical procedures are often necessary to make such comparisons valid. This section provides an overview of the methodological considerations that need to be applied to develop valid species comparisons.

Comparisons of Species Welfare in Captivity

It is important to recognize that individuals within a species have a state of welfare, and this is measurable; however, the species group itself does not have welfare. Individuals within a species may have an overall tendency towards high (positive) or low (negative) welfare in captivity, and here the ‘welfare of a species’ is a short-hand way of referring to these overall trends for individuals within a species to experience a particular welfare state.

Species differ in terms of their natural biology, so direct comparisons between species can often be problematic. For example, consider the situation where ‘r’ selected species have short life spans, large litters, and high infant mortality, while ‘K’ selected species have relatively long life spans, small litters, and low infant mortality (Rockwood, 2006). It is apparent that direct comparisons of captive welfare between these species groups in captivity with such different natural history strategies would not be valid using longevity, litter size, and infant survival as putative indicators of welfare. As well, there may be behavioural differences among species that can confound direct comparisons for other variables, including the measures used to assess welfare. For example, the behaviour of seven species of rodents was recorded in an illuminated arena: a situation commonly known to be aversive for rodents. The chinchillas (Chinchilla lanigera) were very active with frequent defecation, while in contrast, their close relatives the guinea pigs (Cavia porcellus) were huddled and inactive (Glickman and Hartz, 1964). The differing reactions of chinchillas and guinea pigs represent alternative strategies to a threatening stimulus, with the guinea pig choosing a freezing response and the chinchillas choosing a flight response. Similarly, in poor environments some species may become inactive rather than develop locomotor stereotypic behaviours, for example, chinchillas, mice, and horses (Equus ferus caballus) frequently develop behavioural stereotypies, while their close relatives guinea pigs, rats, and donkeys (Equus africanus asinus) do not (Mason and Rushen,

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2006). The inactivity in these cases may reflect a stress response, and does not necessarily indicate better welfare.

From the previous examples it is clear that many species cannot be directly compared for certain welfare indicators. There are three different solutions that can be implemented to address these concerns. One method is to use multiple, independent measures that are sensitive to welfare (Mason, 2010). When these multiple measures independently indicate poor welfare, it increases confidence that there is a welfare concern and decreases the probability that the results are due to intrinsic biological differences. For example, Petter (1975) observed that ring-tailed lemurs (Lemur catta) breed well and have few behavioural or medical problems in captivity while the gentle lemur (Hapalemur alaotrensis) has poor breeding success, high captive morbidity, is generally timid and exhibits many abnormal behaviours in captivity. The logical conclusion from this information is that ring-tailed lemurs have better welfare in captivity than gentle lemurs.

The second approach for developing valid comparative assessments of welfare is to standardize the variables against a ‘gold standard’ population living under ideal conditions (Mason, 2010). This ‘gold standard’ population could be a wild population in a good habitat (such as a habitat without human encroachment, poaching, or extreme environmental factors for that species, such as drought; Mason and Veasey, 2010), or a captive population judged a priori to be doing well in captivity. As an example, to compare breeding successes among species the first step would be to calculate the average breeding success in captivity relative to the species optimum measured in the ‘gold standard’ population. This standardized value for each species is then used to compare different species. An excellent example of this is the use of ‘relative life expectancy’ by Mueller et al. (2011) to look for factors contributing to variation in life expectancies of captive ruminants. First they calculated relative life expectancy (rLE): the ratio of the average life expectancy for each species group in zoos compared to the maximum lifespan ever recorded for each of the 78 species studied. Then they compared rLE to the type of food consumed in the wild and the mating system. It was found that rLE of females correlated with the percentage of grass in the species natural diet and the rLE of males was higher in monogamous species compared to polygamous species. Their approach elegantly solves the problem that species typical longevities are intrinsically related to body mass, with small bodied species tending to have shorter lifespans (even when their welfare is optimal), and large-bodied species tending to have longer lifespans (even when their welfare is not optimal).

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The third approach is to statistically account for factors that contribute to inter-species variability (Mason, 2010). To illustrate, the first step in comparing infant mortality between species would be to identify factors likely to influence infant mortality, such as being more developed at birth or having smaller litter sizes. These variables would then be statistically controlled for in the analyses allowing for the identification of the species with the highest infant mortality after differences in the intrinsic levels of infant mortality have been taken into consideration. As an example of how to statistically account for inter-species variability, albeit not on captive welfare, Sol et al. (2002) studied the introduction success of 69 bird species globally to investigate whether behavioural flexibility is associated with the establishment of these species in novel environments. Their measures of behavioural flexibility were brain size and novel feeding innovations. However, brain size is known to correlate with body size (Gittleman, 1986a), so they calculated relative brain size for species comparisons using residuals of log–log regressions of brain mass against body mass to identify species with large brains while controlling for body size. They found that relative brain size was positively associated with invasion success and pairwise comparisons showed that successful invaders had higher rates of feeding innovations, and concluded that behavioural flexibility is a major determinant of invasion success in birds (Sol et al., 2002). Mueller and colleagues (2011) could have also used this approach instead in their analyses, investigating factors predicting species- typical captive lifespans in zoo ruminants, with body mass as a covariate in all models.

Controlling for Phylogenetic Non-Independence

Another important consideration that needs to be examined when species are directly compared is phylogenetic non-independence. Species averages cannot necessarily be treated as independent data points because related species will share traits due to a common ancestry, a phenomenon termed phylogenetic inertia. Related species may thus cluster together due to shared traits, causing relatedness to be a confounding variable that may hide important relationships or be responsible for observed correlations. Treating species averages from related taxa as independent would thus violate the assumptions of many statistical tests (Felsenstein, 1985) and so possibly inflate Type I and Type II errors (Felsenstein, 1985, Gittleman and Luh, 1992). There are statistical methods available to control for phylogenetic non-independence, the most common approach being the use of independent contrasts (Felsenstein, 1985). For this method the contrasts are calculated as a comparison between

11 taxa at each branch of the phylogenetic tree. Thus, a series of N-1 data points are created that are not confounded by phylogenetic relatedness. Numerous software programs are available to calculate independent contrasts such as the PDAP module (Midford et al., 2005) in Mesquite (Maddison and Madison, 2006) and ‘R’ (www.r-project.org).

Why Focus on Captive Carnivores?

Captive carnivores are very deserving of study for a number of reasons. The sizes and diversity of their populations in captivity have already been described (see ‘Introduction’). Captive carnivores appear to be particularly prone to developing stereotypic behaviours; for example, in a review of the literature Swaisgood and Shepherdson (2005) found that captive carnivores showed significantly higher baseline levels of stereotypic behaviours (greater than 15% of total observation time) than did captive primates (less than 2.5 % of total observation time). Locomotor stereotypies are by far the most common form of stereotypic behaviour observed in captive carnivores (Mason et al. 2007), and include behaviours such as repetitive pacing, route- tracing, swimming, and vertical circling (Clubb and Mason, 2007). Captive carnivores are also often prone to a range of breeding problems. As summarized by Diez-Leon et al. (2013) captive male European mink (Mustela lutreola), black-footed ferrets (Mustela nigripes), giant pandas (Ailuropoda melanoleuca) and some felids have difficulty producing offspring, female black- footed cats (Felis nigripes) and sand cats (Felis margarita) may be acyclic, and infant mortality is high in many species including black-footed ferrets, giant pandas, and African wild dogs (Lycaon pictus). Finally, they are also prone to problems at reintroduction, especially if captive- bred; for example, Jule et al. (2008) found that only 13% of 52 reintroductions using captive- born carnivores were successful, whereas this was increased to 31% of 45 reintroductions when previously wild-caught individuals were released.

Furthermore, carnivores display great species differences in their ability to thrive in captivity, making variation between species a good tool for investigating the origin of welfare problems. These are manifest as marked species differences in stereotypic behaviour and infant mortality within the Felids, Canids, Ursids, Mustelids and Viverrids (see Clubb & Mason 2007); for example, snow leopards (Uncia uncia) and black bears (Ursus americanus) were found to have relatively lower levels of stereotypic behaviour and infant mortality than lions (Panthera leo) and polar bears (Ursus maritimus). These differences are predicted by

12 species-typical home-range sizes, as revealed by the first successful instance of using comparative approaches to investigate captive welfare mentioned above (Clubb and Mason, 2007, Clubb and Mason, 2003). Species differences in captive welfare are also in evidence in the Phocids, a group only recently included in comparative analyses of this Order (see Chapter 2). For example, as summarized by Mason (2010), the walrus (Odobenus rosmarus) has a shorter lifespan in captivity than in the wild, reproduces poorly in captivity, and exhibits intense stereotypic rooting behaviour leading to extensive tusk wear. In contrast, captive grey seals (Halichoerus grypus) have similar survivorship in captivity and the wild, and appear to have few breeding difficulties in captivity.

Overall, Carnivores as a group therefore require research on captive welfare. They are also an ideal model system for addressing research questions using the comparative approaches discussed above (Clubb and Mason, 2003, 2007). Due to the substantial numbers of carnivores in captivity it is possible to get a large sample size for analyses. Furthermore, carnivores are frequently the subjects of behavioural studies (Clubb and Mason, 2007) and there is a complete phylogeny available (Nyakatura and Bininda-Emonds, 2012). Carnivores also exhibit great diversity of life history traits (Gittleman, 1986a, Gittleman, 1986b); for example, species can be aquatic (e.g. Steller sea lion, Eumetopias jubatus), semi-aquatic (e.g. polar bear, Ursus maritimus) or terrestrial (e.g. wolf, Canis lupus) (Bininda-Emonds et al., 2001), and they can be fully carnivorous (e.g. tiger), omnivorous (e.g. coyote, Canis latrans), folivorous (e.g. giant panda) or frugivorous (e.g. kinkajou, Potos flavus) (Nowak, 2005).

Aims of this Thesis

The major aim of this thesis project is to identify risk factors that predict whether different species and populations of captive carnivores thrive or are prone to poor functioning in captivity. The results will be used to further our understanding of animal welfare in captivity, to address the management and conservation issues associated with maintaining carnivores in captivity, and to extend our understanding of the biological mechanisms that underlie abnormalities found in captive animals.

Chapter 2 discusses and builds on the previous work by Clubb and Mason (2003, 2007) and statistically investigates aspects of wild behavioural biology as risk factors for increased

13 captive infant mortality and the severity of stereotypic behaviour in carnivores. Chapter 3 is a comprehensive literature review of the phenotypic changes associated with birth/hatch origin (either wild-or captive-born/hatched) across all species. Chapter 4 statistically investigates birth origin and its interaction with aspects of wild behavioural biology as risk factors for stereotypic behaviour in captive carnivores. Chapter 5 will summarize and synthesize the findings of the previous chapters, and discuss the implications for captive carnivores specifically and more generally address the implications for all captive species.

14

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Chapter Two Wild Behavioural Biology as a Risk Factor for Carnivores in Captivity

Introduction

Carnivore species have evolved within specific environmental contexts: their adaptations for dealing with challenges, their limitations regarding the types of challenges they can surmount, and their requirements for proper functioning and development reflect those natural environments. When individuals of a wild species are born or moved into captivity there are potentially large discrepancies between the captive environment and the natural environments for which they were genetically adapted (see Chapter 3). The extent of these discrepancies and their impacts on individuals will vary among species (Mason, 2010). Carnivore species can be scored based on their natural ecological niches and/or behavioural ecology. These measures may be tested as risk factors predicting whether a particular species will, or will not, thrive in captivity. Additionally, these data can be used to inform requirements for captive habitats to best promote and maintain proper functioning and welfare. This chapter presents the results of such analyses.

Hypotheses that address species-typical differences in carnivore locomotor stereotypic behaviour in captivity have generally focused on wild natural behavioural ecology and/or ecological niches. The main hypotheses, originally summarized by Clubb and Mason (2003, 2007), are described below with new information added when available. In the wild, carnivores engage in various prey search, pursuit and consumption activities (Mason and Mendl, 1997, Mason, 1993, Terlouw et al., 1991) and these are often restricted in captive habitats. In the past, the most widely discussed hypothesis has been that locomotor stereotypic behaviour in captive carnivores (e.g. pacing) results from frustrations related to curtailed natural foraging behaviours in general, particularly the appetitive phases of hunting (Jenny and Schmid, 2002, Hoenig and Gusset, 2010). Other hypotheses relating to foraging behaviour speculate that a species’ tendency towards stereotypic behaviours may be related to having either a specialized or broad diet. On the one hand, Boorer (1972) observed that omnivores like raccoons appeared to adapt well to captivity and related this to their broad diets. In contrast, Morris (1964) and Ormrod (1987) suggested that opportunistic omnivorous animals were more prone to ‘boredom’ and associated behaviour problems when held in captive conditions. In support of this Vickery and Mason (2004) found that Asiatic black bears had more pre-feeding stereotypic behaviour than sun bears, hypothesizing that this may be related to Asiatic black bears having a more

19 seasonally variable diet in the wild. Currently there is insufficient evidence to favour one hypothesis regarding dietary specialization over the others (Mason et al., 2013). Further, there may be a ‘U’ or ‘A’-shaped relationship for dietary specialization such that both dietary specialists and generalists are able to adapt better (or worse) to the captive environment compared to species with intermediate levels of dietary specialization. Thus further research is needed to investigate all of these hypotheses regarding dietary specialization (such as this current study, see below).

Many carnivore species are naturally wide-ranging; for example, Clubb and Mason (2007) calculated the median minimum home-range for polar bears as 1,204 km2 and their median average home-range as 79,472 km2, as compared to an average captive enclosure size of only 836.9 m2 . It has been speculated that polar bears, as well as other wide-ranging species such as the coyote (Canis latrans) and wolf (Canis lupus), may be more susceptible to developing pacing behaviours in captivity due their extensive ranging in the wild (Forthman Quick, 1984, Mellen, 1991, Ormrod, 1987). A similar hypothesis is that wild activity may predict captive stereotypic behaviour. It has been suggested that more active species, such as small carnivores and bears, may be particularly susceptible to the development of locomotor stereotypic behaviour (Morris, 1964, McDougall et al., 2006, Meyer-Holzapfel, 1968, Hediger, 1950, Ormrod, 1987). Lastly, Morris (1964) hypothesised that stereotypic pacing derives from territorial patrolling behaviour. In the wild some carnivore species defend their home-ranges (or portions of their home-ranges) against conspecific intruders to protect resources (Mitani, 1979), while other species do not actively defend their home-range (i.e. core areas of home-range overlap and there is evidence that conspecifics are tolerated). Territorial patrolling may reflect unique motivations and behaviours that are distinct from ranging behaviour associated with large home-range sizes, in fact, it has been found that territoriality is actually associated with smaller home-range size in carnivores (Grant et al., 1992). In captivity many carnivore species exhibit pacing and marking along the boundary of their captive enclosures and it is hypothesized that this could reflect intrinsic motivations to engage in territorial patrolling and defense behaviour (Clubb and Vickery, 2006), even though these behaviours are not needed in the captive environment when conspecifics are prevented from entering their ‘home-range’ by enclosure boundaries.

Clubb and Mason (2003, 2007) tested the above hypotheses to identify aspects of natural behavioural biology that predicted risks of stereotypic behaviour for captive species. They statistically investigated the relationships among key variables (specifically: foraging

20 behaviour, hunting behaviour, dietary specialization, activity level, ranging behaviour, and territoriality) related to life in the wild and locomotor stereotypic behaviours, all stereotypic behaviours combined, and infant mortality. Infant mortality was included in these analyses to address whether these hypotheses predicted if species were exhibiting more widespread issues in captivity, rather than just stereotypic behaviour. Clubb and Mason found that the extent to which a species ranges naturally in the wild was predictive of how that species would respond to the captive environment. Large-bodied, wide-ranging species and those with greater daily travel distances exhibited higher levels of both infant mortality and locomotor stereotypic behaviour, although the latter relationship was not significant when body mass was accounted for. Territorial species also had higher rates of infant mortality in captivity than non-territorial species, but there was no evidence that natural foraging behaviour or activity levels predicted stereotypic behaviour or higher infant mortality.

Ten years of additional data, from studies in both captive and wild settings, have accumulated in the literature since Clubb and Mason (2003, 2007) created, compiled and analyzed their carnivore databases. An additional new source of data has also been created: the database ‘PanTHERIA’ (Jones et al., 2009), which contains information on 5,416 species of mammals for a variety of variables related to ecology, physiology, and behaviour. Furthermore, 10 years ago seals, sea lions and walruses (Pinnipeds) were commonly excluded from phylogenetic analyses of Carnivora due to presumed functional differences from terrestrial carnivores (Fissipeds) (Bininda-Emonds and Gittleman, 2000). However, subsequent investigations found no evidence to support a distinction between pinniped and fissiped carnivores based on functional differences (Bininda-Emonds and Gittleman, 2000, Bininda- Emonds et al., 2001), and as a result pinnipeds are now commonly included in comparative analyses of the Carnivora. In addition, new comparative methods have recently been developed, the Comparative Analysis of Independent Contrasts (CAIC) software has been phased out, and a variety of new comparative, contrast-based programs are available, including Mesquite (see Chapter 1 for details regarding independent contrasts).

New hypotheses have also been put forward to explain species differences in stereotypic behaviour within carnivores. For example, Clubb and Mason (2003, 2007) had suggested that wide-ranging species could be at greater risk in captivity for a variety of specific reasons including the need to perform locomotor behaviours, such as sustained running, that are not possible in captivity; requirements for variation in sensory information from the surrounding environment; requirements for multiple den sites; the lack of cognitive challenges in

21 captivity that sufficiently mimic the spatial and navigational challenges of the wild; or general needs to make decisions and exert control over their environment. Furthermore, a review of the literature by Clubb and Vickery (2006) on carnivore locomotor stereotypic behaviours found that different methodological approaches typically supported specific hypotheses, with no single hypothesis gaining unanimous support. Thus while cross-species analyses have supported a link with natural ranging behaviour, observational studies and environmental manipulations tended to support hypotheses around frustrated natural foraging behaviours or escape responses. Clubb and Vickery (2006) therefore concluded that either the biological traits underlying each of the different hypotheses could be simultaneously important, or that general motivations to escape from aversive, deficient environments may underlie all forms of locomotor stereotypic behaviour. More generally, recent work has also hypothesized that species at risk to anthropogenic changes in the wild may also be more susceptible to the impacts of captivity (Mason, 2010). Traits such as timidity, behavioural rigidity and migratory behaviour all inhibit invasiveness and the ability to thrive in proximity to humans in the wild, and all of these are also thought to be associated with reduced success in captivity (Mason, 2010). Broadly consistent with this idea, in carnivores themselves, large, wide-ranging species are not just at greater risk for increased stereotypic behaviour and infant mortality in captivity (Clubb and Mason, 2003, Clubb and Mason, 2007), but also more susceptible to local extinctions in the wild due to their increased contact with the borders of protected areas (Woodroffe and Ginsberg, 1998). Endangered Canidae have also been reported to have markedly elevated infant mortality in captivity (Ginsberg and Macdonald, 1990).

This current work therefore extends and updates the Captive Stereotypic Behaviour, Captive Infant Mortality, and Wild Carnivore Behaviour Databases to re-examine the hypotheses and conclusions of Clubb and Mason (2003, 2007). The updated databases, expanded with additional species and generating more accurate summary statistics thanks to the inclusion of more recent literature, would have greater statistical power and so could reveal relationships that were not apparent in the original analyses. Furthermore, the association between susceptibility to anthropogenic change in the wild and risk in captivity, a new hypothesis that is testable with available data, will also be investigated. The hypotheses that will be tested and the natural behavioural biology variables and the associated predictions in captivity are summarized in Table 1.

22

Methods

General Overview

Clubb and Mason (2003, 2007) compiled three separate captive carnivore databases which were made available to this study: a Captive Carnivore Stereotypic Behaviour Database, a Captive Carnivore Infant Mortality Database and a Wild Carnivore Behaviour Database (Clubb and Mason, 2003, Clubb and Mason, 2007). These were last amended in 1999, and included both zoo and fur-farmed species. Domesticated species (e.g. dogs) were excluded from the database due to the extensive length of time they have been bred in captivity, and thus adapting to the captive environment. Although zoo and fur-farmed species have also been in captivity for multiple generations, the time-frame domesticated species have been in captivity is substantially greater; for example, it is estimated that dogs (Canis lupus familiaris) were domesticated 11-16 thousand years ago (Freedman et al., 2014), while fur-farmed mink (Neovision vison) have only been bred in captivity since about 1866 (Price, 2002).

Updating the Captive Carnivore Stereotypic Behaviour Database

Data collection

The Captive Carnivore Stereotypic Behaviour Database compiled by Clubb and Mason (2003, 2007) originally contained data for 33 species (Table 2), representing more than 800 individuals, and covering 1960-1999 inclusive. In developing that database the abstracts of all issues of Zoo Biology and the International Zoo Yearbook were manually searched for publications containing data on stereotypic behaviour, as well as the proceedings of the annual meetings of the International Society for Applied Ethology (ISAE). Key researchers in the field also were contacted to obtain relevant published and unpublished data. For the present study, this database was expanded and updated. Additional data on stereotypic behaviour were added from Zoo Biology and the International Zoo Yearbook covering the period 2000-2010, inclusive, using the same methodologies as Clubb and Mason. As well, all issues (from the first issue to 2010, inclusive) of the quarterly zoo animal publication, Shape of Enrichment, and abstracts of the proceedings of the International Conference on Environmental Enrichment and its associated regional conferences were searched. To further enhance the database, the abstracts of three additional journals were searched for all years up to 2010 inclusive: Animal Welfare, Applied Animal Behaviour Science (AABS), and Journal of Applied Animal Welfare

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Table 1. Species characteristics in the wild and hypotheses and predictions for the development of stereotypic behaviour and increased infant mortality in captivity.

Species characteristics Hypotheses Variables Predictions in captivity

Natural foraging behaviour Problems in captivity arise from not being able Time spent foraging Time spent foraging will have a positive correlation with to perform the appetitive phases of hunting stereotypic behaviour and/or infant mortality Vertebrate flesh in diet Percent vertebrate flesh in diet will have a positive correlation with stereotypic behaviour and/ or infant mortality Chase distance Chase distance will have a positive correlation with stereotypic behaviour and/or infant mortality Distance between kills Distance between kills will have a positive correlation with stereotypic behaviour and/or infant mortality Hunt frequency Hunt frequency will have a positive correlation with stereotypic behaviour and/or infant mortality Kill frequency Kill frequency will have a positive correlation with stereotypic behaviour and/or infant mortality Species with a specialized diet will be more Dietary breadth Species with a specialized diet will exhibit more stereotypic prone to problems in captivity behaviour and/or infant mortality Species with a broad diet will be more prone to Dietary breadth Species with a broad diet will exhibit more stereotypic problems in captivity behaviour and/or infant mortality

Naturally high activity levels Species with high activity levels in the wild will Time spent active Time spent active will have a positive correlation with be more susceptible to problems in captivity stereotypic behaviour and/or infant mortality Time spent foraging Time spent foraging will have a positive correlation with stereotypic behaviour and/or infant mortality

Natural ranging behaviour Species that are wide-ranging in the wild are Home-range size Home-range size will have a positive correlation with more susceptible to problems in captivity stereotypic behaviour and/or infant mortality Daily distance travelled Daily distance travelled will have a positive correlation with stereotypic behaviour and/or infant mortality

Territorial patrolling Territorial species are more prone to problems Territoriality Territorial species will exhibit more stereotypic behaviour and/ in captivity than non territorial species or have higher infant mortality

Susceptibility to Species that are at risk of extinction due to IUCN status There will be a positive correlation between the risk of anthropogenic change anthropogenic changes in the wild will also be extinction in the wild and stereotypic behaviour and/or infant susceptible to problems in captivity mortality in captivity

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Science. These were chosen because other meta-analyses have shown that they contain many relevant behavioural studies (Swaisgood and Shepherdson, 2005, Shyne, 2006). This extensive literature search found data on stereotypic behaviour in captivity for an additional 18 species (Table 2). Note that this expanded Captive Carnivore Stereotypic Behaviour Database is annotated by the suffix _2010, and now called Captive Carnivore Stereotypic Behaviour Database_2010, to distinguish it from the original database. The percentage of observation time spent in each type of stereotypic behaviour for each individual was recorded if given; otherwise a group mean was recorded. Other information collected included the age, sex, and birth origin of each individual, where available. Data were entered for more than 450 additional individuals – including many in the original 33 species as well as the new 18 – bringing the database total to more than 1,300 individuals. At least 35% of those individuals exhibited stereotypic behaviour.

Quality control

Studies included in the expanded database were selected carefully, following the methods of Clubb and Mason (2003, 2007). Data were included if the relevant observation period was for at least one full day of data collection (the majority of behavioural studies on captive populations were very short in duration so a more stringent criteria was not used to avoid data loss), stereotypic behaviours were either reported or there was a definitive report stating they did not occur, and the subjects were adults. Studies were excluded if: subjects were food restricted or sub-adult; there had been recent changes to the group structure (including giving birth) or there were recent changes to husbandry or management (for many enrichment studies this meant that the baseline data was used, but not the data once new enrichments were added), so transient novelty effects would not impact the data; animals were intentionally only monitored during periods of frequent stereotypic behaviours; or if the studies were generally poor in quality, for example where there were inconsistencies in how data was recorded between individual animals. The only additional criterion for the 2010 database was the exclusion of studies where the individuals that had been selectively bred as part of the study for decreased stereotypic behaviour (this criteria had not been necessary in the original Clubb and Mason database because these types of studies were not found in their literature search). Individual information, such as ISIS accession number, name, date of birth and sex, was also used to

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Table 2. Species listed in the Captive Carnivore Stereotypic Behaviour Databases, the Captive Carnivore Infant Mortality Databases and the Wild Carnivore Behaviour Databases.

Species listed in the Clubb and Mason New species added to the _2010 databases (2003, 2007) databases

Acinonyx jubatus Canis latrans d Ailuropoda melanoleuca a,b,c Canis lupus d Caracal caracal Catopuma temminckii Felis chaus a,b Eumetopias jubata d Felis margarita Felis manul d Felis silvestris b,d Felis nigripes d Genetta tigrina b,d Halichoerus grypus Hyaena brunnea b,c,d Helarctos malayanus d Leopardus geoffroyi Leopardus colocolo b,d Leopardus pardalis Lontra canadensis b,d Leopardus wiedii b,d Lontra longicaudis b,d Leptailurus serval Martes foina d Lynx canadensis b,d Nasua nasua b,d Lynx lynx Neophoca cinerea b,d Melursus ursinus Odobenus rosmarus b,d Neovision vison d Phoca vitulina Panthera leo Vulpes lagopus Panthera onca Vulpes zerda a,b Panthera pardus Panthera tigris Potos flavus a,b Prionailurus bengalensis a,b Prionailurus viverrinus a,b Puma concolor a,b Puma yagouaroundi a,b Suricata suricatta Tremarctos ornatus a,b Uncia uncial d Ursus americanus a,b Ursus arctos Ursus maritimus Ursus thibetanus Vulpes vulpes

Species with small sample sizes of relevant subjects (N<5) for the following variables were excluded from analyses: a locomotor stereotypic behaviour; b all stereotypic behaviour; c infant mortality; d species with no data specifically for locomotor stereotypic behaviour.

26 identify duplicate entries in the database where the same individual had been part of multiple studies (although some of this information, such as birth date, would be the same between siblings, the combination of information available was complete enough to clearly distinguish individuals). When duplicate entries were found a mean value for stereotypic behaviour was calculated for those individuals following the methods of Clubb and Mason (2007, 2003) so that the final database had only one entry per individual (this was required for ~24% of studies, and mostly involved several zoos where repeated studies were conducted by undergraduate students). Database entries were also randomly chosen to double-check for data entry errors, and none were found.

Only stereotypic individuals were included in the calculation of species medians (see below for how and why these were calculated) due to a general study bias towards studying stereotypic individuals, which would inflate estimates of prevalence and the stereotypic behaviour averages across whole populations. Thus in these analyses stereotypic behaviour is a measure of the average severity of stereotypic individuals rather than the prevalence of stereotypic behaviour in the population. Species were only included in the final analyses if the median for that species represented data from at least 5 individuals (see below for details on how and why medians were calculated). There were no requirements for the number of studies, so if there was only one study for a given species the study mean was used as the median. This criterion is stricter than Clubb and Mason (2003, 2007), where all species were included in the final analyses regardless of how many individuals contributed data to the median (even if only one or two animals).

Calculation of species medians

Each type of stereotypic behaviour recorded was categorized as being ‘locomotor’ (i.e. involving travelling, for example: circling, route-tracing, swimming), ‘stationary’ (i.e. performed in one spot, for example: digging, self-rocking, head circling) or ‘oral’ (i.e. using the jaws, tongue and/or lips, for example: sucking, fur chewing, regurgitation). Study means were calculated for each type of stereotypic behaviour from individual means, and species medians were then calculated from the study means. Medians were used so that very high or very low values from some studies would not be overly influential. The vast majority of the stereotypic behaviours were locomotor: 78% of the stereotypic individuals listed in the database performed at least one type of locomotor stereotypic behaviour, and these were present in at least 45 of the 51 species. In

27 contrast, only 20% of individuals and 10 out the 51 species exhibited non-locomotor stereotypic behaviours. Consequently, species medians for final analyses were calculated for locomotor stereotypic behaviour and for all stereotypic behaviours combined, but not oral or stationary stereotypic behaviour separately since data on the latter were so sparse. Table 3 lists the species medians for stereotypic behaviour and the number of species that had data for each variable, and Table 4 contains information on the sample sizes.

Updating the Captive Carnivore Infant Mortality Database

Data collection

The original Captive Carnivore Infant Mortality Database contained infant mortality data from the International Zoo Yearbook (1988-2000 editions) and fur farms for the 33 species listed in their Captive Carnivore Stereotypic Behaviour Database. The births recorded in their original Captive Carnivore Infant Mortality Database totalled more than 18,000. The International Zoo Yearbook stopped publishing captive infant mortality data in 2000, so the 2010 database could not be updated with more recent information for those 33 species; however, data from the same volumes of the International Zoo Yearbook (1988-2000 editions) were used to generate data for the 18 new additional species. These were extracted using the same methods as Clubb and Mason, i.e., the number of births and deaths of infants under the age of 30 days was recorded for each zoo or breeding facility listed, for calculation of a median (see below). Unfortunately data was not available on the cause of death. With the addition of the 18 new species, the number of births in the Captive Carnivore Infant Mortality Database increased to more than 25,000, with more than 8,900 reported deaths.

Quality control

After the data had been entered from the International Zoo Yearbook, random samples of entered data were double-checked to ensure accuracy. No issues with data entry were discovered. As with stereotypic behaviour, species were only included in final analyses if the median (see below) was calculated from at least five births.

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Table 3. Table 3. Species medians for locomotor stereotypic behaviour, all stereotypic behaviour, infant mortality, and wild variables

Species SBL SBL SBA SBA CIM FOR TRO CHD KID HUR KIR DBR ACT HRS DDT TER EXT ALL SB ALL SB

Acinonyx jubatus 2.94 24.60 2.94 24.60 25.00 3 190.37 1.00 1 16.67 94.38 T 3 Ailuropoda melanoleuca 4.25 5.25 6.50 4.50 50.00 1 3 57.65 3.76 NT 4 Canis latrans 0.00 8.75 44.44 3 200.00 1 51.00 19.91 4.40 T 1 Canis lupus 10.50 10.50 20.00 7.00 3 24.60 0.14 1 43.63 43.13 5.31 T 1 Caracal caracal 12.76 14.74 12.76 14.74 27.27 3 1 275.76 4.90 1 Catopuma temminckii 23.56 23.56 23.56 23.56 16.67 3 1 56.00 2 Eumetopias jubatus 7.20 7.20 46.43 2 6 4 Felis chaus 12.45 12.45 12.45 12.45 40.00 3 1 1 Felis manul 0.00 0.00 90.91 3 1 2 Felis margarita 11.58 12.68 11.58 12.68 20.00 3 1 2 Felis nigripes 0.00 0.00 1.32 3 1 3 Felis silvestris 1.50 1.50 1.50 1.50 28.57 3 1 1.36 1 Genetta tigrina 8.30 8.30 8.30 8.30 21.05 2 6 0.04 1 Halichoerus grypus 51.16 54.64 51.16 54.64 33.33 10.54 3 1.70 2 1 Helarctos malayanus 24.65 24.65 25.59 25.59 40.00 1 3 49.42 3 Hyaena brunnea 12.35 24.70 12.35 24.70 0.00 1.18 2 80.00 9.20 6 42.60 23.38 14.44 T 2 Leopardus colocolo 24.50 24.50 24.50 24.50 56.25 2 Leopardus geoffroyi 11.50 11.50 11.50 11.50 33.33 38.03 0.64 2 Leopardus pardalis 5.50 6.46 5.50 6.46 28.57 3 1 47.30 5.38 3.29 1 Leopardus wiedii 10.44 12.49 10.44 12.49 25.00 3 1 8.01 2 Leptailurus serval 8.42 8.74 8.42 8.74 40.91 6.75 3 0.43 7.50 1 30.10 1.95 2.64 1 Lontra canadensis 4.07 4.07 4.34 4.34 0.00 3 1 58.38 16.95 1 Lontra longicaudis 26.00 26.00 26.00 26.00 63.64 3 2 Lynx canadensis 6.25 6.25 6.25 6.25 19.09 3 46.00 14.60 0.46 1 32.79 1

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Table 3. Continued

Species SBL SBL SBA SBA CIM FOR TRO CHD KID HUR KIR DBR ACT HRS DDT TER EXT ALL SB ALL SB

Lynx lynx 10.83 10.83 10.83 10.83 24.04 3 20.00 7.14 1.63 0.70 1 35.50 137.96 2.17 1 Martes foina 7.77 7.77 0.00 3 1 2.28 1 Melursus ursinus 6.98 15.49 9.53 16.76 33.33 2 6 8.15 1.05 3 Nasua nasua 10.87 43.48 11.37 22.74 29.15 2 6 0.95 1 Neophoca cinerea 23.29 23.29 23.29 23.29 8.33 2 6 4 Neovison vison 4.27 8.13 3.71 9.18 27.92 0.63 1 Odobenus rosmarus 51.27 51.27 51.27 51.27 33.33 2 6 Panthera leo 4.61 9.50 4.61 9.50 42.16 3.00 3 45.00 3.68 1.18 0.22 1 13.00 103.85 11.28 T 3 Panthera onca 17.35 18.69 17.35 18.69 20.00 3 0.17 1 54.30 57.78 4.58 NT 2 Panthera pardus 12.38 10.42 12.38 10.42 25.00 10.38 3 25.18 1.10 0.15 1 40.35 21.08 2.44 T 2 Panthera tigris 10.30 12.96 10.30 12.96 33.33 3 0.13 1 42.75 69.69 T 4 Phoca vitulina 51.15 51.15 51.15 51.15 19.05 3 0.60 1 1 Potos flavus 57.20 57.20 57.20 57.20 0.00 2 4 0.21 1 Prionailurus bengalensis 11.00 11.00 11.00 11.00 33.33 3 1 52.00 1.76 1.30 1 Prionailurus viverrinus 3.44 9.17 3.44 9.17 28.57 3 1 4 Puma concolor 11.75 33.88 11.75 33.88 25.00 3 0.12 1 37.80 138.87 10.35 NT 1 Puma yagouaroundi 3.16 6.04 3.16 7.42 16.67 2 3 49.11 1 Suricata suricatta 10.00 10.00 10.00 10.00 36.84 19.94 3 1 14.06 1 Tremarctos ornatus 52.00 36.00 52.00 36.00 31.67 2 5 53.00 3 Uncia uncia 6.20 6.20 6.20 14.29 3 0.11 1 35.30 24.07 3.23 4 Ursus americanus 15.06 15.06 15.06 15.06 11.11 75.00 1 8.63 1 55.75 34.07 1.63 NT 1 Ursus arctos 6.42 19.90 6.42 19.90 0.00 49.70 2 80.00 6 48.05 333.82 1.55 NT 1 Ursus maritimus 22.75 29.78 20.99 21.87 64.71 15.25 2 3 26.80 82990.48 8.78 3 Ursus thibetanus 0.87 3.81 3.73 7.13 12.50 1 0.29 3 58.05 0.83 3

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Table 3. Continued

Species SBL SBL SBA SBA CIM FOR TRO CHD KID HUR KIR DBR ACT HRS DDT TER EXT ALL SB ALL SB

Vulpes lagopus 0.89 0.55 0.98 0.55 17.20 3 2.85 1 53.00 15.08 T 1 Vulpes vulpes 0.16 0.16 0.16 0.16 22.22 22.50 3 13.71 44.40 1 57.80 3.51 6.45 T 1 Vulpes zerda 4.84 9.68 4.84 9.68 55.00 2 6 1

Total # species 51 43 51 44 51 12 48 9 8 8 10 48 27 33 20 14 49

Gaps indicate no data was available; underlined values indicate medians from fewer than 5 individuals (N<5). SBL, locomotor stereotypic behaviour (% obs); SBA, all stereotypic behaviours (% obs); ALL indicates median for all individuals recorded, SB indicates median for stereotypic individuals only; CIM, captive infant mortality (% births); FOR, time spent foraging (% 24 h); TRO, trophic niche (1: herbivore; 2: omnivore; 3: carnivore); CHD, chase distance (m); KID, distance between kills (km); HUR, hunt frequency (per 24 h); KIR, kill frequency (per 24 h); DBR, dietary breadth (number diet categories consumed); ACT, time spent active (% 24 h); HRS, home-range size (km2); DDT, daily distance travelled (km); TER, territoriality (T, territorial; NT, non-territorial); EXT, risk of extinctions indicated by IUCN status (1, least concern; 2, near threatened; 3, vulnerable; 4, endangered; 5, critically endangered).

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Table 4. Sample size for stereotypic behaviour (number of individuals) and infant mortality data (number of births)

SBL SBL SBA SBA CIM Species ALL SB ALL SB

Acinonyx jubatus 32 8 32 8 844 Ailuropoda melanoleuca 4 3 14 4 4 Canis latrans 12 20 30 Canis lupus 18 18 2061 Caracal caracal 11 10 11 10 406 Catopuma temminckii 5 5 5 5 30 Eumetopias jubatus 7 7 26 Felis chaus 3 3 3 3 395 Felis manul 3 3 45 Felis margarita 11 9 11 9 121 Felis nigripes 2 2 113 Felis silvestris 2 2 2 2 886 Genetta tigrina 1 1 1 1 36 Halichoerus grypus 12 11 12 11 125 Helarctos malayanus 4 4 18 18 60 Hyaena brunnea 2 1 2 1 2 Leopardus colocolo 2 2 2 2 16 Leopardus geoffroyi 12 9 12 9 147 Leopardus pardalis 23 18 23 18 328 Leopardus wiedii 5 4 5 4 51 Leptailurus serval 7 6 7 6 773 Lontra canadensis 2 2 2 2 89 Lontra longicaudis 2 2 2 2 14 Lynx canadensis 2 2 2 2 137 Lynx lynx 10 10 10 10 904 Martes foina 38 38 25 Melursus ursinus 6 5 6 5 71 Nasua nasua 4 1 4 2 1523 Neophoca cinerea 2 2 2 2 7 Neovison vison 334 445 269 Odobenus rosmarus 4 4 4 4 6 Panthera leo 58 10 58 10 2552 Panthera onca 24 18 24 18 494 Panthera pardus 66 27 66 27 580 Panthera tigris 96 28 96 28 2292 Phoca vitulina 10 10 10 10 390

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Table 4. Continued

SBL SBL SBA SBA CIM Species ALL SB ALL SB

Potos flavus 1 1 1 1 114 Prionailurus bengalensis 4 4 4 4 892 Prionailurus viverrinus 5 3 5 3 209 Puma concolor 7 2 7 2 586 Puma yagouaroundi 7 1 7 3 133 Suricata suricatta 5 5 5 5 1983 Tremarctos ornatus 1 2 1 1 148 Uncia uncia 19 21 20 546 Ursus americanus 1 1 1 1 281 Ursus arctos 20 8 20 8 1005 Ursus maritimus 28 26 85 79 263 Ursus thibetanus 64 14 82 50 250 Vulpes lagopus 54 42 54 42 575 Vulpes vulpes 27 11 27 11 599 Vulpes zerda 8 4 8 4 316

Total # species 51 43 51 44 51 # species with N ≥ 5 32 21 34 23 51

Gaps indicate no data was available. SBL, locomotor stereotypic behaviour (% obs); SBA, all stereotypic behaviours (% obs); ALL indicates median for all individuals recorded, SB indicates medians for stereotypic individuals only; CIM, captive infant mortality (% births).

Calculation of species medians

The ratio of deaths over total births for each species was calculated from each zoo or breeding facility and these data were then used to calculate species medians. Table 3 lists the species medians for infant mortality, and the number of species that had infant mortality data, in the updated Captive Carnivore Infant Mortality Database_2010.

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Updating the Wild Carnivore Behaviour Database:

Data collection:

The Wild Carnivore Behaviour Database from Clubb and Mason contained natural behavioural biology information from a literature search covering the years 1960-1999, inclusive, for the 33 species listed in their Captive Carnivore Stereotypic Behaviour Database. A search of key terms including ‘home-range size’ and ‘carnivore’ had been used to identify 18 journals that held the vast majority of articles on carnivore natural behavioural biology (Table 5), and the abstracts of these journals were searched to identify studies with relevant information to create the database.

To update this, wherever possible new species averages were obtained from published databases, rather than through literature searches. This was done to ensure the accuracy of species averages since these databases were compiled from substantive amounts of information by experts in the field. Species averages for home-range size, trophic level (as an estimate of vertebrate flesh in diet, see below for details) and diet breadth were therefore obtained from PanTHERIA (Jones et al. , 2009), while information on IUCN status was obtained from the World Conservation Union Red List (www.iucnredlist.org), and territoriality data came from Grant (1992), which was also the source of the territoriality data used by Clubb and Mason. For other variables, however, new data for behaviour in the wild were obtained by using key words and Web of Science (www.webofknowledge.com) to search the titles and abstracts of all the articles in each of the 18 journals listed in Table 5. The past and present scientific names and all known common names of the 51 species were used as key words (Table 6) to find all the articles in these journals for each species. The article titles and texts of abstracts were then visually searched to identify studies that contained relevant information on behaviour in the wild. In this manner, the database was updated with recent literature (2000-2010, inclusive) for all 51 species, and for the newly added 18 species the literature search was also conducted for the years 1960-1999 since they had not been part of the original Clubb and Mason database (which spanned the years 1960-1999). The following wild behaviour variables were updated using the above methodologies: kill frequency (per 24hrs), hunt frequency (per 24hrs), chase distance (m), distance between kills (km), wild activity levels (% 24 hours), wild foraging (% 24 hours), and daily travel distance (km). After the analyses had been conducted and preliminary results obtained, minimum home-range size (defined as the smallest recorded home-range size) was also obtained by literature search. Following the methods of Clubb and Mason the minimum

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Table 5. Journals used for the wild behaviour literature search

Journal name

Acta Theriologica African Journal of Ecology Arctic Biological Conservation Canadian Field-Naturalist Canadian Journal of Zoology Journal of Animal Ecology Journal of Mammology Journal of Zoology Journal of Wildlife Management Mammal Review Mammalia Oecologia Oikos South African Journal of Wildlife Research South African Journal of Zoology Wildlife Monographs Zeitschrift Saugetierkunde

home-range recorded within each study was used to calculate the median minimum home- range size for each species.

Quality control

To ensure the accuracy of final species averages a selection process was applied to determine which studies would be included in the Wild Carnivore Behaviour Database_2010. Following the methods of Clubb and Mason (2003, 2007), key aspects of each study reported in the literature were examined, including sample size, the method used to obtain data, and age group of the subjects. To be included, each study had to be at least 10 months in duration so that it would span multiple seasons and also had to reference wild, non-provisioned adult populations. For estimates of hunting and kill rate a new criterion was added: studies were excluded when

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Table 6. Search terms used to find wild behaviour information for each species

Species Search terms

Acinonyx jubatus jubatus; cheetah Ailuropoda melanoleuca melanoleuca; panda; giant panda Canis latrans latrans; coyote Canis lupus lupus; wolf; gray wolf Caracal caracal caracal (common name also caracal) Catopuma temminckii temminckii; Asiatic Golden cat; Temminick's Golden cat Eumetopias jubata jubata; Steller's sealion; jubatas; Stellar sealion Felis chaus chaus; jungle cat Felis manul manul; Pallas cat Felis margarita margarita; sand cat Felis nigripes nigripes; black-footed cat Felis silvestris silvestris; wildcat; wild cat Genetta tigrina tigrina; cape genet; blotched genet Halichoerus grypus grypus; grey seal; gray seal Helarctos malayanus malayanus; Malayan sun bear; sun bear; honey bear Hyaena brunnea brunnea; brown hyena Leopardus colocolo colocolo; Pampas cat Leopardus geoffroyi geoffroyi; Geoffroy's cat Leopardus pardalis pardalis; ocelot Leopardus wiedii wiedii; margay Leptailurus serval serval (serval also common name) Lontra canadensis canadensis; North American river otter; northern river otter Lontra longicaudis longicaudis; neotropical river otter; neotropical otter Lynx canadensis canadensis; Canadian lynx; Canada lynx Lynx lynx lynx; Eurasian lynx; European lynx Martes foina foina beech marten; stone marten Melursus ursinus ursinus; sloth bear Nasua nasua nasua; South American coati; ring-tailed coati Neophoca cinerea cinerea; Australian sea lion Neovision vison vison; American mink Odobenus rosmarus rosmarus; Pacific walrus; walrus Panthera leo lion; leo Panthera onca onca; jaguar Panthera pardus pardus; leopard Panthera tigris tiger; tigris Phoca vitulina vitulina; harbour seal; harbor seal Potos flavus flavus; kinkajoo

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Table 6. Continued

Species Search terms

Prionailurus bengalensis bengalensis; leopard cat Prionailurus viverrinus viverrinus; fishing cat Puma concolor concolor; cougar; mountain lion; puma Puma yagouaroundi yaguarondi; jaguarundi; yagouarundi Suricata suricatta suricatta; meerkat Tremarctos ornatus spectacled bear; Andian bear; ornatus Uncia uncia uncia; snow leopard Ursus americanus americanus; American black bear; blackbear Ursus arctos arctos; brown bear; grizzly Ursus maritimus maritimus; polar bear Ursus thibetanus thibetanus; Asiatic black bear; moon bear; white-chested bear Vulpes lagopus lagopus; arctic fox; white fox; polar fox; snow fox Vulpes vulpes vulpes; red fox Vulpes zerda zerda; fennec fox

estimates did not include observed kills or hunts for all prey species since this would underestimate the calculated kill rate and hunt rates. For example, studies were excluded when they only looked at reindeer kills and specifically omitted kills that were monitored/encountered involving other types of prey species. It also was decided that updating the database for proportion of live vertebrate flesh in species’ diets was not worthwhile. The majority of the published studies looked at stomach contents, which does not control for the amount of carrion (thus not live flesh) consumed. This is an important concern for species comparisons because the amount of carrion consumed would differ systematically between species (and involve quite different appetitive behaviours from hunting). Thus, proportion of vertebrate flesh was not used in the analyses. Trophic niche was substituted as a rough estimate of live vertebrate flesh consumed, since this variable was readily available in the PanTHERIA database. As with the stereotypic behaviour and infant mortality databases a random sample of database entries were checked for data entry errors, and none were found.

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Calculation of species medians

Species medians for the wild behaviour variables were calculated in a similar manner to the stereotypic behaviour medians. For each variable, individual values were used to calculate a study mean, and the study means were then used to calculate species medians. Table 3 lists the species medians for the wild behaviour variables and the number of species that had data for each variable.

Statistical Analyses

Controlling for confounding factors

Species medians cannot be treated as independent data points, as related species will share traits due to a common ancestry, a phenomenon termed phylogenetic inertia (see Chapter 1). Treating species medians from related taxa as independent data points would violate the assumptions of many statistical tests (Felsenstein, 1985). This issue can be resolved by calculating independent contrasts between related species and ancestral nodes on a phylogenetic tree, which results in N-1 independent contrasts which are independent of phylognetic relatedness. For this study phylogenetically independent contrasts (Felsenstein, 1985) were therefore calculated using the PDAP module (Midford et al., 2005) in Mesquite version 2.75 (Maddison and Madison, 2006) using a recently updated and complete phylogenetic carnivore super tree (Nyakatura and Bininda-Emonds, 2012).

Across species many natural history variables correlate with body mass (Gittleman, 1985). It is important to take this into account to ensure that observed relationships between the variables are not due to body mass. All variables listed in Table 1 were therefore analysed to determine if they were correlated with body mass (while also controlling for phylogenetic inertia), and when they were, body mass was controlled for in all subsequent analyses by adding it to the statistical models. Body mass effects were also explored in more detail for relationships between home-range size and both stereotypic behaviour and infant mortality. Clubb and Mason found that only when acting together in a least squares regression, were body mass and range size highly predictive. I aimed to find out whether this result held, or whether home-range size statistically controlling for body mass (or vice versa) would now predict locomotor stereotypic behaviour. To statistically control for other variables, a ‘sequential sums of squares’ procedure was used with the term of interest last in the model (Doncaster and

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Davey, 2007). I also investigated whether home-range and body mass together would predict infant motality to replicate the approach used in this previous study. This was done by including both home-range and body mass as factors in a general linear model (GLM) and looking at the significance of the whole model.

Another potential confound which may influence infant mortality is the degree of infant development at birth, i.e. whether altricial or precocial. Altricial infants are notably hairless or sparsely furred, their sensory systems are underdeveloped and their ears and eyes are closed, they lack coordinated locomotion and effective thermoregulation, are nutritionally dependent on their mother, and are born into larger litters of siblings (Thompson et al., 2010). By contrast precocial infants are fully furred, have functional sensory systems, are capable of coordinated locomotion and thermoregulation, are born into smaller litters of siblings, and are less dependent nutritionally on their mother and oftentimes can eat some solid food shortly after birth (Thompson et al., 2010). Altricial infants may have higher infant mortality due to their greater vulnerability than the more developed precocial infants. Schmalz-Peixoto (2003) tested this hypothesis controlling for phylogenetic inertia and found a weak effect showing that altricial young have higher mortality rates in captivity. These differential life history strategies (altricial/precocial) may therefore mask true relationships between captive infant mortality and wild behavioural biology variables under investigation. The relationship between captive infant mortality and the degree of development at birth was therefore analyzed to determine if any are confounds that should be taken into account in subsequent analyses. Degree of development was inferred from the following: litter size, neonate body mass/ adult body mass, age that eyes open, and age weaned, all obtained from the PanTHERIA database.

Clubb and Mason (2003, 2007) found that the method of observation used by studies and captive husbandry were not correlated with any of the variables they investigated, and they did not vary between species. The only exception was enclosure size, which was positively correlated with body mass, but did not predict stereotypic behaviour and so was not a systematic confound. Thus, these variables were not investigated as confounds in the current analyses due to time constraints and the large overlap in data (~2/3 overlap) between the original and updated databases.

Finally, when more than one variable proved predictive, and I had biological reasons to believe that these variables might be inter-related, I re-ran models with both variables included to see which was the main driver of the observed effects.

39

Running the regression analyses

Least squares regression analyses were performed to determine the relative strength of the relationships between the 12 variables listed in Table 1 and locomotor stereotypic behaviour, all stereotypic behaviours combined, and captive infant mortality. The phylogenetically independent contrasts (see above) were exported into JMP 10.0 for analysis, with all regression lines forced through the origin. The latter is necessary because the sign of each x and y value for the calculated independent contrasts is arbitrary (since it does not matter which species or node in a pair is subtracted from the other when contrasts are calculated). The regression line therefore needs to go through the origin since it is the absolute distance of each contrast from the origin that is important, not the positioning of each contrast relative to others (Garland et al., 1992). Univariate analyses were performed since small sample sizes for some variables made the available data insufficient for multivariate analyses. No adjustments needed to be made for polytomies as the carnivore tree is very well resolved for these 51 species. Appropriate transformations were used when necessary to normalise the data to ensure the assumptions of all statistical tests were met. Tests were one-tailed in almost all cases, due to clear directional predictions. Because of this and the large number of tests run, trends are not considered in the Results. The results were also graphed and visually inspected for potential outliers. Outliers were confirmed using an online version of the Grubbs test (http://graphpad.com) with alpha set at 0.05 (two-tailed p-value). Confirmed outliers were removed and data were then reanalyzed (when outliers were removed this is indicated in the tables where the results are reported; all figures show data with outliers removed). Results are given as either T or F-values depending on how JMP reported the output.

Exclusion of poorly sampled species for the stereotypic and wild behaviour variables (to enhance the accuracy of calculated averages) deviated from the method used by Clubb and Mason (2003, 2007). As well, data for many variables were not available for certain species. Altogether this resulted in the final sample sizes being much smaller than the original 51 species for many variables (Table 3 and 4). When analyses were conducted to further investigate the relationships between the variables that were significant in the main analyses, two of these tests would not run due to small sample size. In order to tentatively explore these relationships within the current dataset, these analyses were rerun using all species, even those for which data came from four or fewer individuals. These two analyses are clearly indicated in the text, and all other analyses use medians calculated from at least 5 individuals.

40

Results

Identifying Possible Confounds

Table 1 variables found to correlate with body mass were: trophic level, diet breadth, distance between kills, time spent active, home-range size, and IUCN status. Thus in analyses using these six variables, body mass was added to the statistical models as a covariate. Surprisingly, no significant relationships were found in the data between infant mortality and the altricial/precocial variables (Table 7). Nevertheless, I did still explore these variables as potential confounds to be thorough.

Table 7. Relationship between infant developmental rate and infant mortality

Reproductive variable

Ratio of neonate body mass to adult body mass T=-0.84, p=0.204, d.f.=1,36 a Litter size T=0.86, p=0.196, d.f.=1,44 a Age eyes opened (days) T=1.11, p=0.138, d.f.=1,38 Age weaned (days) T=0.12, p=0.452, d.f.=1,40

All p-values are one-tailed a Outliers removed

Predictors of Stereotypic Behaviour

The relationships between each wild behaviour variable and the severity of locomotor stereotypic behaviour, all stereotypic behaviours, and infant mortality are presented in Table 8. Locomotor stereotypic behaviour was found to positively correlate with chase distance (Figure 1), home-range size (Figure 2), and daily distance travelled (Figure 3). There were no significant correlations between all stereotypic behaviours combined and any wild behaviour variable (Table 7). Furthermore, there were no relationships between IUCN status and locomotor stereotypic behaviour, all stereotypic behaviours or infant mortality (Table 8).

To determine whether the correlations between locomotor stereotypic behaviour and chase distance, home-range size and daily distance travelled (Table 8) were independent effects, each pair of wild behaviour variables were regressed against each other to see if they were interrelated. No significant relationships were found (home-range size and chase distance: T=0.60, p=0.569, d.f.=1,6; home-range size and daily distance travelled: T=0.36,

41 p=0.727, d.f.=1,14; chase distance and daily distance travelled: T=0.05, p=0.965, d.f.=1,5). However, despite this, other studies suggest that they may in fact be interrelated: carnivorous species typically have larger home-ranges (Kelt and Van Vuren, 2001, Hendriks et al., 2009) and daily travel distances (Carbone et al., 2005) than herbivorous species, and body mass is – as well as being correlated with home-range size (Nilsen and Linnell, 2006, Hendriks et al., 2009) – linked with hunting strategy, whereby larger carnivorous species feed on larger prey and invest more energy into hunting behaviour per unit of prey (Carbone et al., 2007). Analyses were therefore conducted to further investigate the relative importance of these three variables (chase distance, home-range size, daily distance travelled) for predicting locomotor stereotypic behaviour in captivity. The wild behaviour variables were regressed against locomotor stereotypic behaviour while controlling for one of the other two variables (and body mass where appropriate). When the relative importance of home-range size and daily distance travelled were investigated, home-range size remained significantly correlated with locomotor stereotypic behaviour when daily distance was controlled for (T=2.20, p=0.032, d.f.=1,7, one-tailed); however, the correlation between daily distance travelled and locomotor stereotypic behaviour became non-significant (T=-1.71, p=0.065, d.f.=1,7, one-tailed) when home-range size was controlled for (the trend is in the opposite direction of the prediction). When relationships between locomotor stereotypic behaviour and chase distance controlling for home-range size, and locomotor stereotypic behaviour and home-range size controlling for chase distance were investigated, there were not enough data for the statistical programs to run the models. The same was true for models investigating the relative importance of chase distance and daily distance travelled. Therefore all species, regardless of the number of individuals contributed to the species median, were now included and these two analyses rerun to tentatively investigate these relationships. Chase distance remained significant when controlling for both home-range size and body mass (T=2.18, p=0.048, d.f.= 1,4, one-tailed), while home-range size effects remained a trend, albeit not quite significant, when analyses controlled for chase distance and body mass (T=1.90, p=0.065, d.f.=1,4, one-tailed). In contrast, both chase distance and daily distance travelled each showed no significant correlations with locomotor stereotypic behaviour when the other variable was controlled for (chase distance: T=1.73, p=0.091, d.f.=1,3, one- tailed; daily distance: T=-0.11, p=0.460, d.f.=1,3, one-tailed).

Following the methods of Clubb and Mason (2003, 2007) the relationship between locomotor stereotypic behaviour and home-range size and body mass together was

42

3.5

3

2.5

2

1.5

1

0.5

0 Locomotor Stereotypic LocomotorStereotypic Behaviour (%obs) 0 10 20 30 40 Chase Distance (m)

Figure 1. Relationship between locomotor stereotypic behaviour (% obs) and chase distance (m). Each data point represents an independent contrast between two species or ancestral nodes.

4

2

0 -1.5 -1 -0.5 0 0.5 1 1.5

-2

-4

-6

Locomotor Stereotypic LocomotorStereotypic Behaviour (%obs) -8 Home-Range Size (km2)

Figure 2. Relationship between locomotor stereotypic behaviour (% obs) and home-range size (km2) controlling for body mass (kg). Each data point represents an independent contrast between two species or ancestral nodes.

43

4

3

2

1

0 -3 -2 -1 0 1 2 -1

-2

-3

-4 Locomotor Stereotypic LocomotorStereotypic Behaviour (%obs) Daily Distance Travelled (km)

Figure 3. Relationship between locomotor stereotypic behaviour (% obs) and daily distance travelled (km). Each data point represents an independent contrast between two species or ancestral nodes.

investigated with least squares regression analyses to determine if being large with a big home- range size is a greater risk factor than just having a big home-range. The relationship was found to be highly significant (F2,13=0.0001, p <0.0001, one-tailed).

Predictors of Infant Mortality

There were no significant correlations between the wild behaviour variables and infant mortality (Table 8), even though Clubb and Mason (2003, 2007) had found significant positive relationships between home-range size and captive infant mortality. However, the methods used here differed from Clubb and Mason (2003, 2007); the latter had used a smaller number of species and had also used minimum home-range size, while in the current analyses mean home-range data were obtained from the PanTHERIA database. Regression analyses across the updated data were therefore repeated using minimum home-range sizes as well as restricting the pool of species to those used by Clubb and Mason (2003, 2007) (Table 9). Captive infant mortality was still not significantly correlated with either minimum or median

44 home-range size in the reduced or full species dataset. Also, to replicate the Clubb and Mason work regression analyses were performed to see if home-range size and body mass together predict infant mortality. This model was significant (Table 9), but within the model the relationship between infant mortality and body mass was highly significant (T=2.70, p=0.006, d.f.=1,26, one-tailed) and appeared to be the variable driving this relationship. To further investigate the apparent loss of relationship between home-range size and captive infant mortality regressions were repeated controlling for the potentially confounding variables listed in Table 7. The relationship between captive infant mortality and home-range size remained non- significant (Table 10).

Discussion

This current study replicates the findings of Clubb and Mason (2003, 2007) for stereotypic behaviour showing that home-range size in the wild is a predictor of locomotor stereotypic behaviour in captive carnivores, and additionally provides several new insights into this relationship. First, it shows that locomotor stereotypic behaviour and non-locomotor forms of stereotypic behaviour (i.e. forms in the ‘oral’ and ‘stationary’ categories described above) have distinctly different predictors, with home-range size predicting locomotor stereotypic behaviour but not overall stereotypic behaviour (a category which includes non-locomotor stereotypic behaviour). Thus, while locomotor stereotypic behaviour comprises the vast majority of the stereotypic behaviour recorded in the database (78% of stereotypic individuals performed at least one type of locomotor stereotypic behaviour and ~90% of all recorded stereotypic behaviour was locomotor) the inclusion of a small proportion of non-locomotor stereotypic behaviour (~10% of total) in the database lead to a non-significant correlation between home- range size and all stereotypic behaviours combined.

Second, the data show that body mass is not a crucial predictor of stereotypic behaviour and home-range size predicts stereotypic behaviour even when body mass is statistically controlled for. This is in contrast to the work of Clubb and Mason (2003, 2007) where home- range size and body mass together (but not home-range size alone) significantly predicted stereotypic behaviour in captivity. Further analysis of the current datasets (Captive Carnivore Stereotypic Behaviour Database_2010 and Wild Carnivore Behaviour Database_2010) also

45

Table 8. Regression analyses between wild behaviour variables and locomotor stereotypic behaviour, all stereotypic behaviours combined and infant mortality

Hypotheses: Problems in Wild behaviour variables Locomotor stereotypic behaviour All stereotypic behaviours combined Infant mortality captivity stem from ...

Natural foraging behaviour Time spent foraging (% 24 hour) T= - 0.35, p=0.370, d.f.=1,5 c T=-0.46, p=0.334, d.f.=1,5 c T=-1.02, p=0.168, d.f.=1,8 c Trophic level T= 0.43, p=0.338, d.f.=1,17 a, c T=0.67, p=0.255, d.f.=1,20 a T=0.12, p=0.453, d.f.=1,44 a

Chase distance (m) T= 4.21, p=0.012, d.f.=1,3 (+) no additional data T=0.10, p=0.463, d.f.=1,6 Distance between kills (km) T= 0.60, p=0.304, d.f.=1,2 a T=0.96, p=0.219, d.f.=1,2 a T=-1.93, p=0.063, d.f=1,4 a

Hunt frequency (per 24 h) T= 1.19, p=0.149, d.f.=1,4 c no additional data T=0.31, p=0.383, d.f.=1,5 c Kill frequency (per 24 h) T= 1.32, p=0.129, d.f.=1,4 T=1.56, p=0.089, d.f.=1,5 T=0.44, p=0.336, d.f.=1,8

Diet breadth d T= 1.54, p=0.143, d.f.=1,17 c, d T=0.43, p=0.668, d.f.=1,19 c, d T=0.51, p=0.611, d.f.=1,44 d Naturally high activity levels Time spent active (% 24 h) T= 0.58, p=0.288, d.f.=1,12 a T=0.08, p=0.470, d.f.=1,13 a T=-1.31, p=0.103, d.f=1,19 a, c

Time spent foraging (% 24 hour) see above see above see above Natural ranging behaviour Home-range size (km2) T= 3.42, p=0.002, d.f.=1,13 (+) a T=1.66, p=0.060, d.f.=1,14 (+) a T=-1.64, p=0.056, d.f.=1,26 (-) a, b, c

Daily distance travelled (km) T= 2.00, p=0.037, d.f.=1,10 (+) T=0.35, p=0.367, d.f.=1,11 T=1.15, p=0.133, d.f.=1,16 c Territorial patrolling Territoriality T= - 0.29, p=0.390, d.f.=1,5 c no additional data T=1.16, p=0.136, d.f.=1,10 Anthropomorphic change IUCN status T=-0.48, p=0.317, d.f.=1,19 a T=-0.25, p=0.405, d.f.=1,19 a T=0.06, p=0.478, d.f.=1,41 a

All p-values are one-tailed unless otherwise indicated a Body mass controlled for b Non-significant, opposite direction of prediction c Outlier removed d Two-tailed tests performed on this variable

46 showed that home-range size and body mass together are more significant predictors of locomotor stereotypic behaviour than home-range size alone with body mass controlled. These data suggest that bigger carnivores with larger home-ranges in the wild are at a much greater risk for locomotor stereotypic behaviours in captivity as compared to smaller carnivores that also are wide-ranging.

Table 9. The relationships between home-range size and infant mortality in carnivore databases

Wild behaviour variables Database Infant mortality

Mean home-range size (km2) 51 species in updated_2010 T=-1.64, p=0.056, d.f.=1,26 (-) a, c database 33 species listed in Clubb et al. T=-0.06, p=0.477, d.f.=1,24 a (2003, 2007) database Minimum home-range size (km2) 51 species in updated_2010 T=-1.10, p=0.143, d.f.=1,20 a database 33 species listed in Clubb et al. T=-1.46, p=0.082, d.f.=1,16 (-) a (2003, 2007) database

2 c Mean home-range (km ) and 51 species in updated_2010 F 2,26=3.633, p=0.021 body mass (kg) database

All p-values are one-tailed a Body mass in model b Non-significant, opposite direction of prediction c Outlier removed

Third, when the interactions between home-range size, daily distance travelled and chase distance were examined (all three of these wild behavioural variables show significant correlations with locomotor stereotypic behaviour) the home-range size effect is persistent even when daily distance travelled was controlled for, but the daily distance effect is no longer apparent when home-range was controlled for. Thus, the travel distance result appears to be just a side effect of range size (and/or possibly chase distance, see below), and not influential in itself. This suggests that the link between home-range size and stereotypic behaviour is mediated by aspects of a wide-ranging lifestyle other than daily active travelling. These aspects are discussed in more detail later.

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Table 10. Relationship between home-range size and infant mortality controlling for reproductive variables.

Reproductive variables

Neonate/adult body mass T=-0.35, p=0.366, d.f.=1,21 a Litter size T=-0.64, p=0.264, d.f.=1,23 a, b Age eyes open (days) T=-1.15, p=0.133, d.f.=1,19 a, b Age weaned (days) T=-0.04, p=0.967, d.f.=1,19 a, b

All p-values are one-tailed a Body mass in model b Outliers removed

In addition, a new, but long-suspected, predictor of stereotypic behaviour emerged from the data, i.e., the typical chase distance employed while hunting prey. Again, it should be noted that this wild behaviour variable only predicts locomotor stereotypic behaviour, and not all stereotypic behaviours combined. This relationship may be independent of the home-range effect, since chase distance was found to predict stereotypic behaviour even when the home- range size is controlled for. However, a major caveat is that when the relationship between home-range and chase distance were analysed the sample size was too small for the statistical tests to run with the cut-off of 5 individuals per species median, therefore all species were included, even those with very poor sample sizes. Thus, this result is tentative, and requires further investigation in the future. The evidence that coursing hunting styles predispose some carnivores to pacing in captivity could help explain why such activities are often triggered by stimuli predictive of food (Mason and Mendl, 1997). Many of the species in the home-range size analyses do not chase prey as their primary means of obtaining food (e.g. grizzly bear, kinkajou, serval), and thus their home-range size is still their crucial risk factor for developing locomotor stereotypic behaviours in captivity. In contrast, the daily distance travelled effect vanished when chase distance was controlled for, and vice versa, further confirming that daily distance travelled is not an independent predictor of stereotypic behaviour.

Several other long-suggested wild behaviour predictors of stereotypic behaviour, including territoriality, naturally highly active lifestyle, and some aspects of hunting behaviour,

48 are once again all not significant (c.f. Clubb and Mason, 2007, Clubb and Mason, 2003). In some cases the lack of correlations may be Type II errors reflecting very small sample sizes, particularly for certain hunting variables (for example, distance between kills: N=5; hunt frequency: N=8; kill frequency: N=6). However, some of the other non-significant variables had substantially larger sample sizes and their results provide further insights into how wild behaviour is, or is not, a risk factor in captive environments. Trophic level, an estimation of the amount of vertebrate flesh in the diet, is not significantly correlated with locomotor stereotypic behaviour in captivity and this suggests that specific aspects of hunting behaviour, not the consumption of vertebrate flesh in and of itself, are the important risk factors. As well, wild activity levels in general did not predict stereotypic behaviour, further indicating that aspects of ranging other than travel and general activity underlie the home-range size relationship with stereotypic behaviour.

When the relationship between the wild behaviour variables and infant mortality in captivity were investigated the results differed from the previous work by Clubb and Mason. Home-range size, daily distance travelled and being territorial were no longer predictors of higher infant mortality. Although the combined effects of home-range size and body mass were predictive of higher infant mortality in captivity, this relationship appears to be primarily driven by the strong positive correlation between body mass and infant mortality. These different results from those of the original work (Clubb and Mason, 2003, Clubb and Mason, 2007) could be due to the addition of more species and individuals, the use of an updated phylogenetic tree, and/or the subtle difference in how Mesquite calculates contrasts compared to CAIC, the software used previously. The current data raise the possibility that the former results (Clubb and Mason, 2003; Clubb and Mason, 2007) were a Type I error, but does support Clubb & Mason (2007)’s suggestion that infant mortality and stereotypic behaviour may have different causal factors. In carnivores the vast majority of infant deaths across 29 species in captivity were related to poor maternal care, including infanticide (Schmalz-Peixoto, 2003). Thus investigating variables that may more directly influence the development of maternal behaviour (i.e. early social experience in dams and how captive and wild social grouping differ) and infanticidal tendencies (i.e. factors that may increase stress in dams, such as close proximity of predatory species) might better explain inter-species variation in infant mortality. Completing additional analyses investigating husbandry variables were beyond the scope of this Masters thesis, but are an important avenue for future research.

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Another possibility is that the current results are Type II errors, and that home-range size, daily distance travelled and being territorial do predict captive infant mortality as was found previously. The inconsistencies between the current and past analyses may result from poor quality data due to difficulties in accurately recording very early infant mortality. For example, one study found that when the nest boxes of mink were monitored by video the recorded infant mortality rates were substantially higher than had been previously estimated (J. Malmkvist personal communication, Dec 1st 2011; and see http://www.agrsci.org/ny_navigation/nyheder/nyheder/the_naked_truth_about_mink_births/). Accuracy in recording infant mortality is likely to be particularly difficult for species that are small-bodied, have small altricial infants or large litters, and could result in data that are skewed towards underestimating infant mortality in those species. Indeed, the positive correlation found between body size and infant mortality may be an artifact of these infants being easier to count and monitor. Another crucial factor that may be impacting data quality is that unlike stereotypic behaviour, infant mortality is also present in wild populations. Thus, wild behavioural biology might be a better predictor of the difference between captive and wild infant mortality compared to just captive infant mortality (see Chapter 1 for details on how to use wild populations as a benchmark to control for inter-species variation in traits in cross-species analyses). Unfortunately data for wild infant mortality data was not available. Many species of carnivores nest in burrows, are nocturnal, and are very cautious of humans (Schmalz-Peixoto, 2003), which makes collecting data on certain variables, such as infant mortality, very difficult. Overall, more research is therefore needed to ascertain for certain what are or are not the predictors of captive infant mortality (a topic returned to below).

No support was found for the recent hypothesis that species which are threatened in the wild are more susceptible to the impacts of captivity: IUCN status did not predict locomotor stereotypic behaviour, all stereotypic behaviour, or captive infant mortality. This result is positive for ex situ conservation efforts, since species threatened with extinction are the ones that would possibly require captive breeding and reintroduction programs. However, species with increased management effort, such as those that are threatened and/or part of captive breeding programs, have been found to do better in captivity than other species (Mueller et al., 2010), thus management factors could be masking any potential relationships between endangerdness status and susceptibility to issues in captivity. Further, there was a strong skew in the dataset towards species that are not threatened with extinction; for example, of the 49 species for which information was available, 35 were classified as ‘least concern’ or ‘near

50 threatened’, but only 8 as ‘vulnerable’, 4 as ‘endangered’, and none were ‘critically endangered’. This is consistent with numerous other studies which have also found that endangered species are actually underestimated in zoo populations (Martin et al., 2014, Maresova and Frynta, 2008, Conde et al., 2013). It would therefore be beneficial to further investigate this hypothesis with data from a larger number of threatened species.

Overall, it appears from these new analyses that wide-ranging behaviours (home-range size) and hunting (chase distance) in the wild are both risk factors for the development of stereotypic behaviour. The results have important implications for housing carnivores in captivity. As Clubb and Mason (2003, 2007) highlighted, there is now sufficient evidence to predict that other wide-ranging species, such as wolverines (Gulo gulo), would be vulnerable to locomotor stereotypic behaviours. They also suggested that thoughtful enrichments need to be devised to meet the particular needs of wide-ranging animals in captivity. These could include access to novel environments, multiple den sites, providing the ability to alter environmental conditions, and allowing activities that stimulate sensory, cognitive or navigational abilities (discussed in more detail below). Furthermore, additional species with long chase distances that are now predicted to be at risk of locomotor stereotypic behaviour include some canids such as African wild dogs (Lycaon pictus). Enrichments that might best be tailored to such species in captivity could involve provision of live prey (although this is ethically problematic), opportunities to chase moving objects (e.g. Quirke et al., 2013), increased exercise in the form of running wheels or treadmills, or perhaps foraging enrichments that promote other forms of appetitive pre-feeding behaviour such as searching for prey or manipulation of prey items prior to consumption: again all topics discussed in more detail below.

These new data thus also raise several interesting and useful research questions for future work. The robustness of the ‘home-range size’ effect opens several avenues for both research and immediate habitat modifications to reduce stereotypic behaviours in captive carnivores, and ideally, also improve their welfare. Issues related to home-range size and stereotypic behaviour in captivity should now be examined in detail to determine the exact features that mediate the causal relationship between these two variables. This could be accomplished either through more detailed comparative analyses or by studying the effects of different types of enrichments. These investigations will provide specific information on which aspects of being wide-ranging (large home-range size) best predict stereotypic behaviour (for example, needs for novelty, utilization of navigation/cognitive abilities, adaptations for sustained locomotion) (Clubb and Mason, 2003, Clubb and Mason, 2007). The combination of being large

51 and wide-ranging is an especially powerful predictor of locomotor stereotypic behaviour in captivity, and since body size is correlated with different types of hunting behaviour (see above), this may reflect the combined influence of hunting and ranging, and further research is needed to either tease apart these relationships, and/or understand how they combine to increase risk. The specific biological traits that underlie the ‘chase distance’ effect should also be investigated to determine how this risk factor can best inform improved husbandry. The underlying features related to stereotypic behaviours could include adaptations for sustained locomotion or needs to express sustained appetitive pre-feeding behaviour. It would also be valuable to examine whether home-range size or chase distance effects rely on experience; for example, are they unique to wild-caught animals with experience of natural ranging or hunting? (see Chapter 4). Furthermore, it should be determined whether home-range size or chase distance predict stereotypic prevalence as well as severity, and whether these wild behaviour variables also act as general predictors of captive welfare (see Chapter 5 for more details).

With respect to non-locomotor forms of stereotypic behaviour, the wild behaviour variables (risk factors) associated with these have not yet been identified. Substantially more data will be required to conduct such analyses. In the current database individuals from only 10 species exhibited stereotypic behaviours that were non-locomotor, and there were insufficient data to investigate stereotypic behaviours in the oral or stationary categories separately. So far, we know that different phylogenetic groups tend to exhibit specific forms of stereotypic behaviour. While locomotor stereotypic behaviours are common in carnivores, ungulates tend to perform oral forms (such as tongue rolling) (Mason and Rushen, 2006), and these differences seem to reflect variations in natural lifestyle (Bergeron et al., 2006, Mason and Mendl, 1997). Recent research on other taxa has linked different forms of stereotypic behaviour with varying biological risk factors. Pomerantz (2013) found that daily travel distance predicted pacing across species of primates in captivity, while sociality in the wild predicted hair pulling. Furthermore, time-consuming food search behaviour in the wild predicts feather damaging behaviour in captive species of parrots, while large brain volumes predict both oral and whole body stereotypic behaviours in this same group (Kinkaid et al., 2014). An understanding of the risk factors for each category of stereotypic behaviour within carnivores would help shed light on why different species and different phylogenetic groups vary in the types and severity of stereotypic behaviours they tend to perform, and also help identify enrichments that might best reduce non-locomotor stereotypies.

52

Future research should focus on filling in the data gaps within the current analyses to thoroughly investigate which – if any – of the other natural behavioural biology variables are risk factors for captive carnivores. It is still unclear whether IUCN status, territoriality, or other aspects of hunting behaviour truly have no predictive role or correlation with stereotypic behaviour, or whether more and better quality data are still needed. It may prove particularly fruitful to investigate the hunting variables since many of these had a small sample size in our database. Examination of hunting variables that are not measures of distance could also help determine if the severity of locomotor stereotypic behaviours in captivity stems from adaptations for sustained locomotion in the wild. Unfortunately, it can be challenging to obtain behavioural data for species that are elusive, small, or live in dense habitats. Another difficulty is that the manner in which carnivores are being studied appears to be changing. There are increasing numbers of studies using GPS or satellite technology to monitor wild animals, and fewer relying on traditional tracking or direct visual observation. These newer technologies change the type of information available. While GPS or satellite tracking may give a lot of important information regarding large scale movements and behaviours, these types of studies are not able to differentiate or describe many of the behavioural details, such as the amount of time spent foraging or hunting frequency.

The current dataset will lack sensitivity and specificity for identifying risk factors due to variability in the data resulting from variation in data collection methods. Creating a standardized methodology that addresses the key issues in data quality that could be universally adopted would be beneficial. For example, the quality of the stereotypic behaviour data would also be improved with more 24 hour studies to get more complete behavioural profiles for individual animals in captivity. Currently, many behavioural studies on stereotypic behaviour only cover the period of time the zoo or facility is open, which could underestimate the amount of stereotypic behaviour in nocturnal or crepuscular species and overestimate it in diurnal species. As well, most stereotypic behaviour studies are short in duration (often only days in length), even though it has been shown that stereotypic behaviour does vary seasonally (e.g. Carlstead and Seidensticker, 1991). For the variables on behaviour in the wild the database was comprised of studies that spanned at least 3 seasons, which improves data quality, but this was not possible or the stereotypic behaviour database. Increasing the number of behavioural studies focused on a wider behavioural range of individuals, rather than only the stereotypic individuals, would also allow for the true prevalence of stereotypic behaviour to be studied and compared between species, rather than just severity measures of stereotypic

53 individuals. As well, expanding the species breadth in captive carnivore studies would also be beneficial, since the current work is biased towards felids (24 of the total 51 species in the database, and 13 of the 21 species used in the locomotor stereotypic behaviour analyses).

The collected infant mortality data in the current analyses arguably had a sufficiently large sample size (49 out of 51 species), but as discussed previously, there are some concerns about the data quality. Additionally, information on cause of death would also be valuable. Species that are kept more intensely (such as fur-farmed species, and those involved in more intense captive breeding programs for conservation purposes) may be more susceptible to disease, but this potential confound could not be evaluated with the current dataset. A newer source of higher quality data is needed to properly determine if the previous biological correlations with infant mortality described by Clubb and Mason (2003, 2007) were Type I errors, or if the lack of significant results in our current analyses are Type II errors. Notably, the International Zoo Yearbook stopped updating its database with records of infant mortality in 2000. The ISIS database, which annually compiles data from zoos around the world, is one possible resource that could be used to obtain the required data to repeat the infant mortality analyses (such data were requested for the current project, but ISIS did not want to collaborate and provide the necessary data).

Turning to more fundamental questions, chase distance and home-range size appear to be independent predictors of locomotor stereotypic behaviour in captivity, but it is unclear whether or how they act in combination. Research is needed to see whether or not they have additive effects, and if so, how they do this. One basic unknown is whether chase distance and home-range size both predict a shared, common behavioural outcome, or whether ranging and coursing hunting style (long distance chasing) instead each predict different sub-types of locomotor stereotypic behaviour. In other words, we do not know whether they both predict the same behaviours in captivity, or whether they actually each predict subtly different forms which we have erroneously pooled into one category. More detailed data on the morphology and timing of locomotor stereotypic behaviours are needed to resolve this. It would be particularly relevant to compare species that have relatively small chase distances and large home-ranges (e.g. Eurasian lynx and lions) to those with relatively large chase distances and small home- ranges (e.g. cheetah and coyote) to specifically identify whether the form of the locomotor stereotypic behaviour they exhibit are similar or different. Were chase distance and home- range size found to have additive effects on a common behavioural outcome, with both predicting exactly the same stereotypic behaviours, research would then be needed to

54 investigate how. One possibility is that home-range size and hunting style both predict adaptations within the animal that promote stereotypic behaviours. For example, Vickery and Clubb (2006) suggested that species may be more prone to develop more severe stereotypic behaviour in captivity when they have an inherent ability to sustain locomotion. While this explanation may now seem less likely, given that daily distance travelled appears to be just an artifact of home-range size, and that general activity levels did not correlate with stereotypic behaviour, it could still be that abilities or motivations to perform particular types of locomotion (trotting, loping or running) are what mediate the links between ranging, chasing and performing locomotor stereotypic behaviour. A second possibility is that natural tendencies to range and chase both predict effects in captive animals that then give rise to locomotor stereotypic behaviour. For example, if being wide-ranging or chasing prey in the wild both lead to frustration in the captive environment, this could increase escape motivations and thence predispose both sets of species to more locomotor stereotypic behaviour. Another possibility is that being raised in captive environments where ranging or hunting opportunities are denied both alter CNS development in ways that predispose individuals to developing stereotypic behaviour. Evidence does suggest that captive-bred animals may be more prone to stereotypic behaviour, while wild-caught individuals may be more stressed, fearful and frustrated (see Chapter 3); thus, comparisons of captive-born and wild-caught populations according to the strength of the relationships between stereotypic behaviour and the two wild behaviour variables could help distinguish if the underlying mechanisms in both effects involve abnormalities in the CNS, are related to stress/ fear/ frustration, or differ between the two predictors (see Chapter 4).

In summary, evidence was found to support the hypotheses that aspects of wild hunting behaviour (chase distance) and ranging behaviour (home-range size and daily distance travelled) are risk factors for developing locomotor stereotypic behaviours in captive carnivores (but not other forms of stereotypic behaviour). Species that invest more in hunting and are wider-ranging thus tend to exhibit more severe stereotypic behaviours. The relationships between ranging and hunting behaviour appear to be independent, with hunting behaviour being the slightly more important risk factor, but being both wide-ranging and large-bodied the strongest risk factor of all. Further research is needed to investigate the relationship between specific components of hunting or ranging and stereotypic behaviour to provide a more comprehensive understanding of the impacts of these variables. Future research should also focus on increasing data quality by increasing the breadth of species examined, filling in data gaps for the wild behavioural variables, and improving data quality for stereotypic behaviour and

55 infant mortality.

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Chapter Three The Effects of Birth or Hatch Origin: How Wild Versus Captive Developmental Environments can Affect Phenotype within a Single Generation

Introduction

It is likely that for many species the issue of birth or hatch origin – whether individuals begin life and develop in captivity or in the wild – has long-term and diverse effects, because wild and captive environments are fundamentally different in many respects. While it is important to note that these are generalizations, and specific captive and wild environments will vary according to husbandry and habitat quality. For example, most animals in captivity are housed in cages or enclosures that are dramatically smaller than the territories they would occupy in the wild (see Chapter 1). The diets of captive and wild animals also may differ substantially, with captive diets tending to be less diverse, more processed, more reliable, and having larger portions than wild diets. This not only impacts the nutrition an animal receives, but also the behavioural, cognitive, physical and physiological activities involved in obtaining or processing food (Swaisgood and Shepherdson, 2005). Other behavioural opportunities may be restricted in captive animals including choice of mate, social companions and group structure, dispersal and migration. Overall, the captive environment is less complex, less stimulating and provides fewer opportunities for performing species-typical behaviours. However, on the positive side, animals in captivity generally have not only greater access to food, but also to water, veterinary care and protection from predation (Mason et al., 2013).

There is much speculation and some concern about differences between individuals differing in birth or hatch origins. For example, there is a growing awareness that the welfare of wild animals brought into captivity may be reduced compared to captive-born or hatched conspecifics. This led the European Union to recently pass legislation banning the use of wild- caught individuals in scientific research (Council of the European Union, 2010). Similarly, there is considerable debate surrounding the welfare implications of selling animals caught in the wild as exotic pets (e.g. http://www.exotic-pets.co.uk/about-wild-caught-exotic-pets.php). In other contexts there is, conversely, great concern for the well-being of captive-born or hatched individuals, notably when they are released into the wild as part of species recovery plans (Hunter et al., 2013, Balmford et al., 1995). Finally, in scientific studies captive-born or hatched animals are used frequently to model natural processes and learn more about their wild

60 conspecifics, yet, if birth origin effects are not clearly understood these research findings may not be valid beyond the captive laboratory population (Mason et al., 2013).

Considerable experimental research shows that an animal’s early experiences and the environment in which it develops can have lasting impacts on its phenotype (Langford et al., 2014, Sih, 2011). The underlying process whereby one genotype can express multiple phenotypes is referred to as phenotypic plasticity (West-Eberhard, 2003), and that range of possible phenotypes is called the reaction norm (Stearns, 1992). Phenotypic plasticity can be intrinsic to some genotypes, with some species having a greater potential for phenotypic plasticity than others (Pigliucci, 2005). A particular phenotypic state can be either developmentally permanent or labile, sometimes referred to as either ‘irreversible’ or ‘reversible’ plasticity respectively (Sih, 2011), but most cases fall on a continuum between these two extremes (Sih, 2004). These phenotypic changes have also been classified as adaptive, maladaptive, or malfunctional (Mills, 2003). Adaptive traits are a normal expression of the phenotypic variation, and help the animals to cope, or even thrive, in the current environment. Oftentimes fitness can thus be maintained through a range of environmental deviations. However, at a certain point fitness will drop as abnormalities develop (Monaghan, 2008). A trait classified as maladaptive represents normal phenotypic variation, but does not improve fitness in the current environment, often because the organism developed in preparation for a different environment (Mills, 2003). Malfunctional traits represent true pathology (Mills, 2003) and result from deviations from the expected experience or developmental plan when certain conditions required for proper development and functioning are absent (Rutter and O'Connor, 2004).

The objective of this review was to systematically review the literature to comprehensively identify all aspects of phenotype (including behaviour, morphology, physiology, health, and life-expectancy) documented to be impacted by birth/hatch origin. Several published reviews have focused on the impacts of an animal’s early life experiences on its adult phenotype, teasing apart interactions between the early and late environment (Monaghan, 2008). Additional studies related to my focus have compared wild-born or hatched animals that are living in the wild with captive-born or hatched animals maintained in captivity (O'Regan and Kitchener, 2005, Saragusty et al., 2014, Bello-Hellegouarch et al., 2013), thus combining developmental effects with immediate environmental effects. Others have reviewed the processes involved in the domestication of wild animals in captivity, genetic as well as developmental (Price, 1999). Further, a recent review of the literature examined domestication- like effects that occur rapidly when wild animals are moved into captivity (Mason et al., 2013).

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Studies have also examined the changes that occur when domestic animals are released back into the wild, a process referred to as ‘de-domestication’ (O'Regan and Kitchener, 2005, Price, 2002, Koene and Gremmen, 2000), and again genetic as well as developmental. These all highlight how some of the previously noted differences between captive or wild born/hatched animals in captivity may be due to factors unrelated to birth or hatch origin per se; for example, genetic changes, influences of the current adult environment, or to other factors. To date, there has been no review that systematically synthesizes the literature to specifically examine the effects of a wild or captive birth or hatching, and associated development in those environments, on the phenotype of an individual. In this review we are therefore interested in the lasting phenotypic features of individuals that are associated with their birth or hatch origin, and their corresponding development and maturation in either captive or wild environments. This developmental time frame includes parental influences, gestation/pre-hatch development, birth/hatching and development from the neonatal phase all the way through to sexual maturity. This range was chosen because the effects of the environment during these periods of development can be profound due to sensitive periods or ‘open developmental windows’ (Sih, 2011). During these periods phenotypes can be altered more easily and permanently than after sexual maturity and during adulthood.

To properly identify and describe true at that time birth/hatch origin effects that reflect altered development due to environmental influences, it is therefore important that confounding factors are identified and minimized. In many published studies, for instance, authors compare individuals harvested from wild populations to individuals from captive populations that had been maintained for many generations in captivity (Calkins et al., 2013, Nogueira et al., 2004, McCleery et al., 2013). In some of these comparisons, the observed differences between the wild- and captive-born or hatched individuals may therefore have resulted from genetic differences between the populations due to differential selection pressures, or even from founder effects in the establishment of the original captive populations (Williams and Hoffman, 2009). Such genetic effects are not the focus of this review. In addition, for some species aspects of phenotypes remain surprisingly plastic into adulthood. Some of these labile characteristics may appear at first to be birth or hatch origin effects, but in fact, they may more accurately reflect variations in that individual’s current living conditions. For example, the digestive organs of many wild birds are longer and larger than those of captive birds; however, these are diet-dependent differences that appear rapidly at any age, regardless of developmental background or stage of development. The smaller digestive tracts of

62 captive-hatched birds therefore rapidly change to resemble those of their wild conspecifics after release into the wild, provided they survive long enough in the wild (Moore and Battley, 2006). Again, these rapid, stage-independent phenotypic responses to current environments are not relevant to this discussion. The present review thus aims to identify specific birth/hatch origin developmental effects on individuals while teasing out other confounding factors.

Methods

To specify definitions, in this review individuals are referred to as being ‘captive-bred’ or ‘wild- bred’ and these designations indicate where that individual’s life began (either born or hatched) AND where a large portion of development to maturity occurred (Figure 1). Ideally this time frame would begin at conception or fertilization so that influences occuring during development in the womb or egg would be included. Unfortunately, conclusively identifying the environment at conception or fertilization would be impossible in most cases since this information is rarely included in published studies. ‘Wild-caught’ individuals are a subset of the wild-bred population transferred to captivity after birth or hatching (Figure 2). ‘Captive-reared’ individuals were in contrast born or hatched in the wild but transferred to captivity early in life (infancy or depending on the species an equivalent early developmental stage) and then reared in the captive environment; similarly, ‘wild-reared’ individuals were born or hatched in captivity but then reared in the wild environment (Figure 1 and 2). The methods of collecting information were as follows. Relevant studies of non-human animals were found by conducting a literature search using the search engine Web of Science (www.webofknowledge.com) with the search terms ‘captive-born’, ‘wild-born’, ‘captive-bred’, ‘wild-bred’ and ‘captive AND wild’ (as one search term). These searches generated a list of several thousand papers that were then examined for birth/hatch origin data. All abstracts and titles were scanned to identify papers that might contain information relevant to this review, promising papers then being read in full. Other opportunistically encountered papers containing birth/hatch origin data also were included. Several criteria were applied in selecting studies for inclusion, to minimize the impacts of the confounding factors discussed above, as well as to ensure that birth/hatch origin comparisons were based on high quality data rather than anecdotal observations. First, relevant studies were those that directly compared wild-bred and captive-bred animals in the same, or very similar, environments to control for differences that may be due to environmental factors and not

63 birth/hatch origin. Thus, while there will be variability within captive and wild environments for factors such as husbandry and habitat quality, this would not cause systematic differences between the populations being compared (wild-bred and captive-bred). The next set of criteria aimed to address the possible problem of population level genetic differences between groups. Studies were included if the captive-bred individuals were the first generation born or hatched in captivity (F1), or if a large proportion of the population (at least 2/3) of the captive-bred population was F1 (Figure 1 and 2). Thus, studies were included if these involved captive-bred F1 individuals released into the wild for comparisons with wild-bred conspecifics in situ, or captive-bred individuals now in the wild compared with their F1 wild-born offspring (Figure 1 and 2). All studies involving individuals from populations maintained in captivity for multiple generations were excluded, in contrast. If the number of generations in captivity was not explicitly stated in a publication’s Methods section, then that particular breeding program, institution and species were investigated more thoroughly for clarification, and when necessary, assumptions made based on the available information. For example, if individuals came from a farm or long-term captive breeding program, then multiple generations in captivity were assumed and these studies were excluded. If the captive breeding program had been operational for only a short period of time relative to the reproductive generation times of the species in contrast, it was assumed that a large proportion of the captive-bred animals would be F1 individuals, and those studies were included. Studies of individuals who were born or hatched in one environment (captive or wild) but transferred to the alternate environment (wild or captive) early in development (during infancy or an equivalent early developmental stage) were included in the category in which they were reared, not born or hatched, since the majority of their development took place in that rearing environment. Supporting this, evidence indicates that individuals who are transferred from one environment to another early in development typically resemble the phenotype of their rearing environment in terms of behaviour and morphology (Schultz et al., 2009, Schaller, 1972). The specific details in such cases are noted in the text. In order to control for labile phenotypic changes, birth origin studies were included only if the captive- and wild-bred individuals were resident in the same or equivalent environments for those comparisons. Other confounds that could impact the birth/hatch origin effects were noted during the literature survey. These included hand-rearing, premature maternal separation, and social isolation; another issue that was encountered involved age differences between wild-caught and captive-bred individuals since often the captive-bred individuals were the offspring of wild-caught individuals. These studies were included, but the

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Figure 1. Diagram illustrating key definitions relating to wild-bred individuals, as well as the comparisons used between captive-bred and wild-bred animals in the wild environment to examine phenotypic plasticity while minimizing effects due to environmental and/or genetic factors.

Figure 2. Diagram illustrating key definitions relating to captive-bred individuals, as well as the comparisons used between captive-bred and wild-bred animals in the captive environment to examine phenotypic plasticity while minimizing effects due to environmental and/or genetic factors.

65 confounding issue is noted in the text.

All differences between captive-bred and wild-bred populations reported in this review are statistically significant unless otherwise noted. When authors did not statistically investigate birth/hatch origin effects and raw data were available, appropriate statistical analyses were performed and the details were noted in the text as a footnote. When raw data were not available, reported differences were noted as anecdotal evidence, untested hypotheses, or expert opinion. In general, the examples provided within each subsection and topic (see below) progress from anecdotal or less reliable data where there are confounding factors, to data involving differences in rearing history but not actual birth/hatch environment, to true birth/hatch origin data that were not statistically analyzed, with each section then concluding with the most rigorous statistically significant comparisons of wild- and captive-bred subjects. The conclusions in each section are weighted most heavily by these more rigorous studies. This allowed for the inclusion of a wider variety of studies, while also retaining the integrity of the conclusions since poorer quality studies were noted. Overall, information and data on birth/hatch origin effects covered natural behaviour patterns; stress and fear responses; many aspects of reproduction; somatic physiology and anatomy; brain development and cognition; abnormal behaviours, such as stereotypic behaviour; and morbidity and mortality. Each of these is covered next, after which I discuss potential mediators and mechanisms.

Birth/Hatch Origin Effects

1) Natural Behaviour a) Foraging behaviour

Several studies have looked at foraging behaviour, and specifically foraging efficiency/abilities. Behavioral observations found that captive-hatched Atlantic salmon (Salmo salar) released into the wild chose less efficient feeding sites than wild conspecifics (Orlov et al., 2006), while steelhead trout (Oncorhynchus mykiss) originating from a hatchery and released into the wild showed more surface-oriented foraging behaviour, resembling captive feeding responses, compared to their wild conspecifics (Simpson et al., 2009). Similarly, captive-born golden lion tamarins (Leontopithecus rosalia rosalia) were less efficient at foraging when reintroduced into

66 the wild: they spent more time handling and manipulating food items during foraging than the first generation (F1) of wild-born tamarins (Stoinski et al., 2003). Furthermore, captive-hatched ring-necked pheasants (Phasianus colchicus) were more reliant on supplemented food after their release than wild-hatched pheasants (Bright and Morris, 1994, Bagliacca et al., 2008), and across 17 species captive-born carnivores released into the wild were more likely to die of starvation than translocated wild-born conspecifics1 (Jule et al., 2008), suggesting poor foraging abilities – though a caveat of this last study is that only some captive-born individuals were likely to have been F1, while the others probably came from populations bred in captivity for multiple generations. In tests, captive-born animals also have been found to be less efficient foragers than wild-caught conspecifics brought into the laboratory. For example, a study examining wild- caught brown trout (Salmo trutta) found that they fed more efficiently on live prey than hatchery- reared trout (Sundstrom and Johnsson, 2001). As well, in jumping spiders (Portia audax) wild- caught individuals were more likely to orient towards prey items on a video-screen than captive- hatched individuals (Carducci and Jakob, 2000).

Prey selection has also been found to differ between captive- and wild-bred individuals. In a study where rearing environments differed, but not hatch environment, fry were hatched from wild honmasu salmon (Oncorhynchus rhodurus X masou) eggs, reared in captivity and later released into the wild as 7 month old parr. Inedible food items such as plants and pebbles were found in the stomach contents of hatchery-reared individuals but not wild-reared salmon, although this difference was statistically significant only for the first few weeks following release (Munakata et al., 2000). Steelhead trout observed in the wild showed marked differences in prey choice depending on their origin: captive-hatched fish from hatcheries consumed fewer salmonids and more invertebrates (Simpson et al., 2009). There were also significant differences in browse preference between the captive-born and wild-caught (both mother- reared) black rhinoceroses (Diceros bicornis) (Ndlovu and Mundy, 2008), where wild-caught individuals consumed more browse overall and captive-born individuals consumed smaller amounts of two of the five types of plants examined.

Other studies have in contrast reported no effects of birth origin on foraging. Starting with a study investigating the effects of post-hatch environment, fry from steelhead trout eggs laid in captivity to wild-caught parents were hatched and reared in either the captive environment or in a wild environment for several months, before the fry were moved into a laboratory to observe feeding behaviour. No differences in feeding rates were found between

1 This study did not statistically control for phylogenetic relatedness

67 the two populations in this laboratory comparison (Riley et al., 2005). In other laboratory experiments it was found that captive-hatched and wild-caught blue crabs (Callinectes sapidus) consumed equal numbers of clams in feeding trials (Davis et al., 2004). As well, wild-caught and captive-born bank voles showed no differences in time spent feeding, handling food (rat chow pellets) or drinking (Cooper and Nicol, 1996), while at a primate research facility, there were no significant differences between wild-caught or captive-born chimpanzees (Pan troglodytes) in leaf swallowing behaviour, a method of parasite control exhibited in wild populations (Huffman and Hirata, 2004).

In summary, birth/hatch origin differences have been documented for foraging behaviours. In cases where differences have emerged, the captive-bred animals generally showed diminished or suboptimal foraging behaviour compared to their wild-bred conspecifics: less efficient and/or involving inappropriate diet selection, and were more prone to starvation when released into the wild.

b) Anti-predator behaviour

Differences in anti-predator behaviour between populations having the same environment at the start of life (born or hatched) but then reared under contrasting conditions (either wild-reared or captive-reared) from an early developmental stage are examined first. In one study of fish, captive-bred and reared brown trout appeared to have heightened anti-predator responses compared to captive-bred conspecifics reared in the wild: the former increased their heart rates more quickly when exposed to a predator, and maintained higher heart rates afterwards (Sundstrom et al., 2005).

By contrast, most studies comparing captive-bred and reared individuals with wild-bred and reared individuals were not consistent with this previous finding. A meta-analysis examining translocated carnivores found that captive-born individuals were more susceptible to predation in the wild (Jule et al., 2008), though as mentioned above, for this study some captive- born individuals may have been derived from a multiple generation captive-breeding program. Additional studies where the captive-born generation was known to be F1 showed similar depressions in anti-predator behaviour compared to wild-born conspecifics. For example, guppies (Poecilia reticulata) bred and reared in the laboratory originating from a high-predation stream had a reduced response to predator models compared to wild-caught parent stock

68 tested with the same models (Kelley and Magurran, 2003); shoals of captive-hatched sea bass (Dicentrarchus labrax) aggregated and reached cohesiveness more slowly in response to eels and overhead predator stimuli, compared to wild-hatched conspecifics tested the same way (Malavasi et al., 2004, Malavasi et al., 2008); and captive-hatched blue crabs were more susceptible to predation when released into the wild, perhaps because they were less likely to bury themselves in the sediment: an anti-predator behaviour (Davis et al., 2004). In the laboratory, captive-born rhesus monkeys (Macaca mulatta) exhibited shorter latencies in reaching for food items in the presence of a live snake or snake-like objects (such as a snake model), and their reactions were rated as ‘less emotional’ than wild-caught subjects (Joslin et al., 1964). However, additional studies show no significant differences between captive-bred and wild-bred individuals for certain aspects of anti-predator behaviour. For example, in the guppy study described above, there were no differences in anti-predator behaviour between captive-born guppies and their parent-stock for the population originating from a low-predation stream (Kelley and Magurran, 2003). Additionally, there were no differences in responses to models of mammalian predators between captive-born and wild-caught Vancouver Island marmots (Marmot vancouverensis), or between captive-born and wild-caught wallabies of two species (Aepyprymnus rufescens and Leontopithecus rosalia rosalia) (McLean et al., 2000, Blumstein et al., 2006). Age was a confounding factor in the marmot study, however, with captive-born individuals being younger than wild-caught individuals.

In summary, only one study showed a heightened response to predators in captive-bred populations and four showed no differences, while five studies showed hindered or depressed anti-predator behaviour in captive-bred individuals. Thus, it appears overall that, when it is effected, anti-predator behaviour is likely to be lower in captive-bred animals compared to their wild-caught conspecifics.

c) Behaviours related to movement, dispersal, and habitat selection

The initial comparisons described here are between individuals with different rearing conditions, but similar hatch environments (see next paragraph for studies where birth/hatch origin and rearing environment differ). The behaviour of rheas (Rhea americana) from eggs that were laid in the wild, but hatched and reared in captivity and then released into the wild, did not differ in their habitat selections from wild native rheas (Bellis et al., 2004). Similarly, blue crabs hatched in the wild, reared in captivity, and then released back into the wild, did not differ from native

69 wild crabs in terms of the depth of the water they occupied in various locations (Davis et al. , 2004).

In contrast, studies looking at populations that differed in both birth/hatch and rearing environments did generally show effects of origin on these behaviours. Captive-born canyon mice (Peromyscus crinitus) seemed to perform more wheel-running in lab cages than their wild- caught parents, although the result was confounded by age (Brant and Kavanau, 1965): the captive-born individuals were much younger (mean age: 3.4 months) than the wild-caught individuals that had been in captivity for 24 months (Brant and Kavanau, 1965). Wild-caught adult voles and African striped mice (Rhabdomys) were also less active than captive-born F1 conspecifics (Cooper and Nicol, 1996, Jones et al., 2011b). Perhaps because some forms of inactivity reflect fear, a topic reviewed below, this effect contrasts with many other studies showing hindered climbing and locomotor abilities in captive-bred individuals compared to wild- bred individuals. Captive-born golden lion tamarins released into the wild showed a reluctance to climb on flexible materials, make long arboreal jumps, or deviate from straight line movements (Menzel and Beck, 2000). They also fell more frequently, used very small and very large branches less, stayed lower in the trees, and were more likely to be found on human- made structures than the first generation wild-born tamarins (Stoinski et al., 2003). Similarly, captive-born deer mice (Peromyscus maniculatus) in the laboratory were less likely than wild- caught conspecifics to climb artificial trees (Pulsifer and Herman, 1989). Examining dispersal, captive-hatched ring-necked pheasants and captive-born dormice (Muscardinus avellanarius) released into the wild, both dispersed smaller distances than wild-born conspecifics that had been relocated (Bright and Morris, 1994, Bagliacca et al., 2008). In contrast, another study found that released captive-born lizards were more active and more likely to disperse over longer distances than native lizards that had not been relocated (Santos et al., 2009).

Some studies found no differences between populations differing only in early rearing history and not place of birth or hatching, however most showed pronounced birth/hatch origin effects for movement, locomotion and habitat selection. In captivity, wild-caught individuals appear to have depressed activity compared with their captive-bred conspecifics; however, captive-bred individuals consistently showed impaired climbing abilities, while the activity levels of captive-bred individuals released into the wild had mixed results.

70 d) Nesting/sheltering behaviour

Several studies have examined birth/hatch origin differences in nesting and sheltering behaviour. In Atlantic salmon, captive-reared fish from eggs laid in the wild were found more likely to share shelters with other fish at higher densities than was normal for wild-reared individuals (Griffiths and Armstrong, 2002). Consistent with the previous sub-section on anti- predator responses, the authors hypothesized that the aberrant sheltering behaviours of these captive-reared fish would likely increase predation risk (Griffiths and Armstrong, 2002). The nesting behaviour of chimpanzees has also been studied. Bernstein (1962) examined the nest- building behaviour of individual chimpanzees and observed that wild-caught animals were more likely to build nests. The results of this study were not analyzed statistically; however, a similar study by Videan (2006) confirmed that wild-caught chimpanzees were significantly more likely to construct nests. This nest-building observed by Bernstein (1962) occurred even when the wild- caught chimpanzees had been brought into captivity as infants, suggesting that certain aspects of nest-building behaviour were acquired very early in life. These studies also examined the complexity of nest building. Wild-caught individuals were found to use more intricate nest- building techniques than their captive-born conspecifics (Bernstein, 1962, Videan, 2006). In groups of captive chimpanzees more nests were also observed in outdoor enclosures when wild-born females were present (Fultz et al., 2013), suggesting that those individuals built more nests.

Thus in studies examining nesting and sheltering behaviours (albeit from only two species and four studies) captive-born individuals had altered – possibly sub-optimal – sheltering behaviour and less complex nesting behaviour than wild-born conspecifics.

e) Self-directed and comfort behaviour

No differences were found for self-directed behaviours, such as self-grooming, yawning, and self-scratching, between wild-caught and captive-born red-capped mangabeys (Cercocebus torquatus torquatus) (Reamer et al., 2010). In contrast, another study found that wild-caught adult voles spent more time grooming, especially preceding periods of inactivity, than their captive-born conspecifics (Cooper and Nicol, 1996). There is thus insufficient evidence to determine if birth/hatch origin effects self-directed and comfort behaviours.

71 f) Social behaviour

Most studies examining birth/hatch origin and subsequent social behaviour have looked at differences between individuals that began their life (i.e. were born or hatched) in the same environment, but were then reared in different environments from a very young age, and later compared in the same environment. In steelhead trout fry, for example, there were no differences in the rate of aggressive behaviour towards conspecific fry from individuals that had been reared in captivity or in the wild (Riley et al., 2005). In contrast, wild-caught juvenile Atlantic salmon were more dominant, and successfully outcompeted and obtained territories from those brought into the lab at the fertile egg stage and reared there (Metcalfe et al., 2003). A similar effect was found for Coho salmon (Oncorhynchus kisutch), where captive-reared individuals (taken into captivity directly after hatching) were typically out competed by wild- caught salmon for breeding opportunities (Berejikian et al., 2001, Berejikian et al., 1997). Another study compared spiny lobsters (Jasus edwardsii) hatched in the wild, reared in captivity, and then released back into the wild, to their wild-hatched conspecifics. The captive- reared lobsters allocated more time to ‘unnecessary’ aggressive behaviour with conspecifics; this ‘unnecessary’ aggressive behaviour had no apparent goal to access resources, and was thought to potentially increase susceptibility to predation due to increased conspicuousness (Oliver et al., 2008).

Only two studies examined differences in social behaviour between populations that differed in both birth and rearing environments (true captive-born versus wild-born according to the definition above). In one, captive-born carnivores released into the wild had greater mortality rates than translocated wild-born conspecifics, due to intra-species aggression (Jule et al., 2008) (as mentioned previously however, it is unknown what proportion of the captive-born individuals were F1). In contrast, computer simulations of groups of captive chimpanzees based on data from their social interactions predicted no differences in group cohesion following removal of either captive-born or wild-caught individuals, suggesting no major differences in social behaviour between these two groups in the community (Leve et al., 2013).

In summary, the few studies demonstrating effects of birth/hatch origin and early rearing history on social behaviour typically found that captive-born or captive-reared individuals are out-competed in social interactions. Although one study found increased aggressive behaviour in captive-reared individuals, this behaviour had no apparent benefits. These findings suggest that aggression and behaviours related to competition may be compromised in captive-bred

72 individuals. Such findings are likely relevant to sexual and maternal behaviour too, topics reviewed in detail below.

2) Stress and Fear in Response to Anthropogenic Stimuli

Captive-bred or captive-reared individuals typically tend to be less fearful of people. For example, starlings hatched in the wild and brought into captivity as nestlings for hand-rearing were less fearful of humans than conspecifics brought into captivity as juveniles (Feenders et al., 2011). Even when captive-bred individuals are not hand-raised they may be less fearful: zookeepers rated captive-born black rhinoceroses as more friendly towards keepers than wild- caught individuals (Carlstead et al., 1999). Conversely, wild-caught Norway rats (Rattus norvegicus) and their F1 offspring had equally strong defense reactions towards people when chased down a runway and when touched or picked up, suggesting no differences between these two groups in fear of humans (Blanchard et al., 1986).

Other studies have examined the fear of non-human but man-made stimuli in wild- caught and captive-bred individuals. In the case of the starlings discussed above, those caught when they were older showed greater escape motivation in novel environments (Feenders et al., 2011). As well, these starlings appeared more neophobic to novel colours on operant device pecking keys (Feenders and Bateson, 2013), although in novel object tests the groups did not differ (Feenders et al., 2011). Similarly, wild-caught African striped mice spent more time in dark compartments in an experimental apparatus, took longer to emerge, and spent more time in the nest box than captive-born F1 individuals (Jones et al., 2011b): manifestations of fear that may explain their low activity levels reported earlier.

An examination of physiological parameters related to stress showed that wild-caught captive coyotes (Canis latrans) had higher serum neutrophils and lower lymphocytes, a condition referred to as a ‘stress leukogram’, than individuals raised in captivity (Rich and Gates, 1979), suggesting that they were sensitive to capture stress associated with blood withdrawal and/or had higher baseline cortisol levels (Rich and Gates, 1979). Note that in this comparison the captive-reared coyotes were taken from their mothers at a young age (before 4 weeks) and hand-raised. In another study, serum glucose levels were elevated in wild-caught owl monkeys, possibly indicating elevated corticosteroids (Weller et al., 1994); however, age

73 was a confound in this study, with captive-born individuals being younger than the wild-caught conspecifics.

Additional studies with better controls have also compared wild-caught individuals in captivity with F1 captive-bred conspecifics. These showed links between being wild-born and physiological signs of increased stress in captivity. Similar to the coyote study above, wild- caught Canadian lynx (Lynx canadensis) had higher serum neutrophile levels/concentrations and lower lymphocyte levels/concentrations than captive-born individuals (this time not hand- raised) (Weaver and Johnson, 1995). In the African striped mice study mentioned previously, wild-caught individuals had higher corticosterone metabolite levels (Jones et al., 2011b). As well, in 11 species of parrots corticosteroid response was more prolonged after restraint in wild- caught birds than in their captive-hatched F1 offspring2 (Cabezas et al., 2013). Baseline fecal cortical metabolites have also been found to be higher in wild-caught animals than captive-born conspecifics in marsh deer (Blastocerus dichotomus) and southern white rhinoceroses (Ceratotherium simum) (Christofoletti et al., 2010, Metrione and Harder, 2011). Likewise, a zoo population of spider monkeys comprising 34% captive-born had substantially higher fecal and salivary cortisol levels than populations where all were captive-born (Ange-van Heugten et al., 2009). However, the opposite trend was observed in woolly monkeys, where a zoo population with only 70% captive-born individuals had lower fecal cortisol levels than all captive-born populations (Ange-van Heugten et al., 2009).

Overall, evidence indicates that wild-caught animals are more stressed in captive environments (most apparent in the appearance of physiological markers of stress), compared to captive-bred conspecifics. Additionally, studies also found evidence that wild-caught animals are also more fearful of humans and anthropogenic stimuli.

3) Reproduction a) Sexual and reproductive development

For some species, captive-born individuals appear to reach sexual maturity and the age of first reproduction earlier than their wild-caught counterparts. Wild-caught squirrel monkeys (Saimiri sciureus) were thus older when they reached sexual maturity, as well as younger at their last

2 This study controlled for phylogenetic relatedness

74 reproduction; however, these differences were not analyzed statistically (Zimbler-Delorenzo and Dobson, 2011). In orcas (Orcinus orca), wild-caught females had their first birth at a mean age of 13.44 years while the only captive-born female to reproduce during this study gave birth to her first calf at age 8 (Duffield et al., 1995). Of the wild-caught females, 93% were captured at 6 years of age or younger, so it is unlikely that this result is confounded by the wild-caught females producing calves in the wild prior to entering captivity. Analyses of birth records from European and American captive populations of chimpanzees and bonobos (Pan paniscus) by De Lathouwers et al. (2005) also found that for captive-born chimpanzees the mean age of the first birth was significantly earlier than for wild-caught individuals. This pattern does not hold for all species however. De Lathouwers et al. (2005) examined the birth records of captive bonobos and found no differences for age at first reproduction between captive-born and wild- caught individuals. Finally, in terms of the age at which females cease breeding, Asian elephant (Elephas maximus) captive-born females in timber camps were found to cease reproduction much earlier than wild-caught females, although the authors did not consider this a robust result since few elephants survived to the age of apparent reproductive cessation (Mar, 2007).

It appears that captive-bred individuals may sometimes reproduce at an earlier age than wild-caught conspecifics, although this was not true for all species examined. Only two studies examined the age at which reproduction ceased, with conflicting results.

b) Reproductive behaviour

Many studies have examined effects of birth/hatch origin on specific aspects of reproductive behaviour. Courtship and copulatory behaviours in six species of gibbons were similar between captive-born and wild-caught individuals raised in captivity, although all had previously been subject to premature maternal separation3 (Mootnick and Nadler, 1997). As previously mentioned (see above, ‘Social behaviour’), captive-reared Coho salmon (taken into captivity directly after hatching) were out-competed by wild-caught salmon, so failing to breed with spawning females (Berejikian et al. , 2001, Berejikian et al. , 1997). Furthermore, female salmon showed a preference for wild-caught males: effects thought to be mediated by differences in secondary sexual characteristics (Berejikian et al. , 2001, Berejikian et al. , 1997).

3 This study did not statistically control for phylogenetic relatedness

75

Some rigorous studies on reproductive behaviour, with fewer confounds, help paint a clearer picture. In aquaria, males from the founding wild-caught population of Lake Malawi cichlids (Tramitichromis intermedius) and the captive-hatched F1 generation both exhibited apparently appropriate courtship behaviours accompanied by sound production (Ripley and Lobel, 2004) as well as exhibiting similar spawning behaviours (Ripley and Lobel, 2005); however, the timing of spawning was different, with wild-caught males showing a mid-day peak while captive-born males exhibited no daily peak. In captive-bred black tiger prawns (Penaeus monodon), hatch-origin effects on reproduction were much more pronounced, with reproductive failure common for captive-bred individuals. In one study 60% of the wild-caught tiger prawn pairs mated successfully, whereas none of the captive-hatched pairings mated successfully (Marsden et al., 2013): an effect largely due to problems with courtship and copulatory behaviour in both sexes, with captive-hatched females being less attractive to the males, and captive-hatched males being less receptive to female cues (Marsden et al., 2013). A similar pattern has been observed in captive giant pandas (Ailuropoda melanoleuca), where the sexual behaviours of captive-born individuals, particularly males, are disturbed, while wild-caught individuals who matured in the wild mate readily (personal communication to Georgia Mason, Kati Loeffler, Nov 1st, 2010).

Many published studies thus reveal birth/hatch origin effects on reproductive behaviour, with captive-born individuals from many species showing some behavioural anomalies perhaps akin to the social deficits reviewed earlier.

c) Reproductive disorders and physiology

Even in situations where individuals exhibit normal courtship and copulatory behaviour, the reproductive success of captive-bred and wild-caught individuals may differ. Across sixteen species of lizards in the genus Varanus, captive-bred individuals had much higher instances of reproductive disorders than wild-caught individuals, although this difference was not examined statistically4 (Mendyk et al., 2013). Similarly, captive-born F1 female white rhinoceroses have lower reproductive success than wild-caught individuals (see below, ‘Overall reproductive output’); F1 females showed normal estrus and sexual behaviour, and males did not exhibit a preference for wild-caught over captive-born F1 females, suggesting that the reproductive failure occurs post-copulation (Swaisgood et al., 2006). Brady et al. (2013) conducted gene

4 This study did not statistically control for phylogenetic relatedness

76 expression and histological analyses of black tiger prawn ovarian tissues, and found higher expression of a major egg yolk protein precursor in wild-caught individuals. This may further account for the greater reproductive output of wild-caught prawns than captive-hatched individuals in these crustaceans (in addition to the courtship and copulation issues previously discussed, see ‘Reproductive behaviour’ above). In contrast, for captive mongoose lemurs (Lemur mongoz) there were no significant differences in testicular sizes between wild-caught and captive-born males during the breeding season, despite substantial differences in reproductive success (see below, ‘Infant mortality and parental care’) (Perry et al., 1992). Similarly, there was no birth origin effects on fertility in either captive chimpanzees or bonobos (De Lathouwers and Van Elsacker, 2005).

In summary, birth/hatch origin effects are sometimes associated with quantifiable reproductive physiological differences between captive-bred and wild-caught individuals: where they differ, captive-bred individuals tend to develop reproductive abnormalities that negatively impact their reproductive output.

d) Infant mortality and parental care

Parental birth/hatch origin influences infant mortality rates in a wide variety of species. For these discussions, measures of infant mortality include fertile eggs failing to hatch, miscarriages, stillbirths, and neonatal deaths. The only study examining birds looked at piping plovers (Charadrius melodus) in the wild. Infant mortality was higher for captive-reared piping plover parents than wild-hatched reintroduced parents. The wild plovers therefore hatched and fledged more young than the captive-reared birds due to this decreased infant mortality, even though both groups laid similar numbers of eggs (Roche et al., 2008).

Within primates, infant mortality rates typically appear higher for the offspring of captive- born parents than for those of wild-caught parents. In mongoose lemurs and black-and-white ruffed lemurs (Varecia variegata) wild-caught mothers had lower infant mortality rates than captive-born mothers (Perry et al., 1992, Schwitzer and Kaumanns, 2009). Similarly, captive- born Callitrichidae primates tended to have poorer parental skills than wild-born individuals (Gengozian et al., 1978, Kingston, 1976). Specifically, in saddleback (Saguinus fuscicollis illigeri) and cotton-top tamarins (Saguinus oedipus), infant mortality and miscarriages were higher for captive-born parents (Wolfe et al., 1975). However, in contrast, in another study on

77 cotton-top tamarins, infanticide was suspected in two of the four wild-caught pairs that bred while the single pair of captive-born individuals that bred successfully raised all their young (Evans, 1983). A caveat for all of these examples is that the authors did not statistically examine these birth origin effects.

However, two primate studies were found that did statistically analyze their data. Similar to the studies above, when twenty-four years of breeding records were examined for chimpanzees used in biomedical research, wild-caught females were rated as being more competent mothers than captive-born females who had been left with their mothers for one to twelve months (followed in turn by females who had been removed from their mothers at less than one month of age) (Brent et al., 1996). In contrast, analyses of captive populations of chimpanzees and bonobos found no significant differences between captive-born and wild- caught populations for rates of abortion, stillbirths, mortality of live-born infants, or number of offspring surviving to 5 years of age (De Lathouwers and Van Elsacker, 2005).

For other groups of mammals, data are sparse. In a study involving nine species of captive-born and wild-caught ungulates (zebra, Equus burchellii; pygmy hippopotamus, Choeropsis liberiensis; kudu, Tragelaphus strepsiceros; wildebeest, Connochaetes taurinus; Eld’s deer, Panolia eldii; reindeer, Rangifer tarandus; giraffe, Giraffa camelopardalis; scimitar- horned oryx, Oryx dammah; and dorcas gazelle, Gazella dorcas) infant mortality was elevated significantly for captive-born dams only in Eld’s deer with no significant difference for the other species5 (Ballou and Ralls, 1982). Infant mortality was also found to be higher for captive-born Indian rhinoceros dams than for wild-caught dams (Zschokke and Baur, 2002). However, there are some counter examples. In a population of Myanmar timber elephants the trend was reversed, with wild-caught dams having 30% higher infant mortality than captive-born dams (Mar, 2007). Similarly, wild-caught female carnivores had more infanticide than captive-born females (Schmalz-Peixoto, 2003). The cause of infanticide also varied with birth origin here, being more likely to be neglect by wild-caught mothers rather than the active killing of young that occurred when captive-born mothers were infanticical.

Overall, relationships between birth origin and infant mortality or parental care are thus not clear cut. In a number of studies parental care and infant survival were better for wild-bred than captive-bred parents; however, there are also several documented cases of the converse.

5 This study did not statistically control for phylogenetic relatedness

78 e) Offspring differences

It is widely recognized that parental phenotype can impact offspring characteristics through mechanisms that – for example – allow for adaptive phenotypic responses to varying environmental conditions (Mousseau and Fox, 1998); thus offspring characteristics can reflect the phenotype of their parents. Parental birth origin has also been found to affect the phenotype of their offspring in captive animals (the wild-caught individuals producing F1 offspring, the captive-born F1 individuals producing F2 offspring). Dennis et al. (2007) found that in black rhinoceroses, wild-caught dams were more likely to produce male calves than captive-born F1 dams, with the incidence of producing male calves increasing with time in captivity, although this result was not analyzed statistically. As well, a final interesting finding is that laboratory-hatched fry from captive-reared Coho salmon were more dominant than laboratory-hatched fry from wild-caught females. This maternal effect appeared to be linked to decreased pigmentation in the fry from captive-reared females, and an inability to signal subordination (Berejikian et al., 1999).

Birth origin effects were thus found for two characteristics of the offspring of parents differing in origin (but themselves born into the same captive environment): sex ratios, and variability in aggressive behaviours likely linked to morphological differences.

f) Overall reproductive output (mechanisms unknown)

It has been noted that captive-bred individuals have poorer reproductive success in captivity than their wild-caught counterparts, particularly in the F1 generation. For example, Carlstead and Shepherdson (1994) reported that in some species (notably great apes and some ungulates) captive wild-born individuals appear to have higher reproductive success than their F1 captive-born offspring. Similarly, the first generation of captive-born mongoose lemurs and Callitrichidae primates have been reported to breed poorly compared to wild-caught individuals, although these differences were not examined statistically (Schaaf and Stuart, 1983, Kingston, 1976). In the case of white rhinoceroses in captivity, twice as many wild-caught individuals bred successfully than captive-born F1 individuals, although again this result was not examined statistically (Versteege, 2007). Others have also reported that wild-caught white rhinoceros dams produced twice as many calves as captive-born dams, although again these data were not analyzed statistically, and the authors were not able to assess management parameters to

79 rule out causes related to breeding opportunities (Dennis et al., 2007). Wild-caught squirrel monkeys exhibited higher fertility than captive-born individuals; however, these differences were not analyzed statistically (Zimbler-Delorenzo and Dobson, 2011). In contrast, in fruit flies (Ceratitis capitata) in the laboratory, wild-caught females laid fewer eggs than captive-reared females from wild-caught pupae (Papadopoulos & Carey, unpublished data cited in Carey et al., 2008). Additionally, for Asian elephants in timber camps, fecundity was significantly greater for captive-born females compared, to wild-caught females, for the age categories prior to the cessation of the captive-born females’ reproduction (Mar et al., 2012).

In other species birth/hatch origin does not appear to affect fecundity in captivity. A multi-institutional study of 20 species of small felids found that birth origin was not a determinant of reproductive success6 (Mellen, 1991). Similarly, snowy plovers (Charadrius nivosus) from wild eggs that were hatched and reared in captivity and then released into the wild, had similar reproductive rates to their wild conspecifics (Neuman et al., 2014), and as discussed above, wild and released captive-reared piping plovers laid similar numbers of eggs (Roche et al., 2008). There were also no differences in the number of infants produced by captive-born lowland gorillas (Gorilla gorilla gorilla) compared to their wild-caught conspecifics when infants born per year of reproductive opportunity were compared (Beck and Power, 1988), although a confounding factor was that a certain proportion of the wild-born individuals likely were brought into captivity as infants and hand-raised (Gould and Bres, 1986).

There are caveats and concerns with all of the above mentioned examples, but close examination of some more rigorous studies helps to clarify the relationships between birth/hatch origin and reproductive success. It was found that significantly more wild-caught female Tasmanian devils (Sarcophilus harrisii) produced offspring than captive-born females7 (Keeley et al., 2012). Similarly, life-time reproductive success, as estimated by the number of returning offspring for each individual, was greater for wild-hatched than captive-hatched Coho salmon, and also greater for captive-hatched, wild-reared than captive-hatched, captive-reared Coho salmon (Theriault et al., 2011). In contrast, the captive-born F1 generation in black-and-white ruffed lemurs had larger litters than the wild-caught founding generation (Schwitzer and Kaumanns, 2009).

Overall although some studies found no differences, two of three rigorous studies found

6 This study did not statistically control for phylogenetic relatedness 7 Analyzed from data presented in paper [x2 (1, N = 46) = 18.05, p <0.0001]

80 a strong birth/hatch origin effect for greater reproductive output in captive wild-caught individuals than captive-bred.

4) Physiology and Morphology

Several studies have investigated the effects of birth/hatch origin on physiology and morphology. Many of those looking at anatomy focused on fish. For instance, differences were found in the secondary sexual characteristics of Coho salmon, where wild-caught males had brighter colors and other enhanced features such as increased snout length as compared to males from eggs laid in the wild but reared in captivity (Berejikian et al., 2001, Berejikian et al., 1997): a finding very relevant to the previous section too. As well, first-generation hatchery- reared Chinook salmon (Oncorhynchus tshawytscha) released into the wild had shallower mid- bodies, longer and deeper heads, shorter post-bodies, and wider anal fins, than wild individuals in the same population (Busack et al., 2007). In another study, captive-bred steelhead trout smolts were larger than wild-caught fish (Simpson et al., 2009). Similarly, captive-bred ring- necked pheasants, marmosets and tamarins were heavier than wild-caught conspecifics (Bagliacca et al., 2008, Kingston, 1976), although it is not known if the differences were statistically significant for the marmosets and tamarins. Additionally, in Livingstone's fruit bat (Pteropus livingstonii) captive-born individuals were more obese than wild-caught adults (Courts, 1999). In contrast, captive-bred rattlesnakes were smaller as neonates than similarly aged wild-caught conspecifics (Brown et al., 2007), although this could be due to stress in the wild-caught dams since they were brought into captivity while gravid. Not all studies found that body structures showed clear birth origin effects however. For example, in Rodrigues fruit bats (Pteropus rodricensis) no musculo-skeletal differences were found between wild-caught colony founders and their captive-born descendants (Kitchener at al, 1999 cited in O'Regan and Kitchener, 2005); while in blue crabs no differences were found between captive-hatched and wild-caught crabs in molting rate or growth increment per molt (Davis et al., 2004).

As previously discussed data from many species show that wild-caught individuals have physiological signs of increased stress in captivity (see above, ‘Stress and Fear in Response to Anthropogenic Stimuli’). The only additional physiological comparison found in the literature examined differences across a wide variety of parameters in wild-caught and captive-born owl monkeys (Weller et al., 1994). Serum protein, glucose and sodium were elevated in wild-caught individuals, while urine calcium and calcium clearance were reduced. The authors suggested

81 however these differences were not due to birth origin per se but to a confound: the younger ages of the captive-born animals than the wild-caught (thus causing their higher metabolic rates, lower adipose tissues, and continued skeletal growth and remodeling).

In summary, captive-bred and wild-caught individuals often differ in both morphological as well as physiological status, with captive-bred animals often being heavier, and wild-caught animals often showing, as already reviewed, classic signs of a physiological stress response in captivity. However, confounding factors such as age may lead to erroneous conclusions; and overall the diverse effects reported do not fall into any clear patterns.

5) Brain Development, Behavioural Organization and Cognition

Two studies have examined cognitive performance in individuals with identical hatch environments but contrasting rearing environments (captive-reared or wild-reared). One looked at long-term memory in snails (Lymnaea stagnalis) and found that captive-hatched and wild- caught individuals performed similarly (Orr et al., 2008). In the other, starlings that had been brought into captivity as nestlings and hand-reared were compared to wild-caught juveniles; again no differences in a learning task were found (Feenders and Bateson, 2013). In this latter study, however, observations suggested that captive-reared starlings were less impulsive, as measured by how delayed rewards were discounted by the individual. The authors hypothesized this could indicate that emotionally-mediated decision-making was altered by rearing experience (Feenders and Bateson, 2013).

Several neurological and cognitive studies also compare wild-caught and captive-bred F1 individuals. Brain size in guppies was compared between a wild-caught founder population and their captive-born offspring: captive-born individuals had smaller brains (Burns et al., 2009). Another study found that wild-caught chimpanzees learned and performed problem-solving tasks (Morimura and Mori, 2010) and tool-use tasks (Brent et al., 1995) more successfully than their captive-born conspecifics, independent of their previous experiences with objects or physical abilities. Similarly, in jumping spiders, wild-caught individuals performed better in insight-learning tests that examined efficiencies in reaching a prey item (Carducci and Jakob, 2000), while captive-born female common marmosets (Callithrix jucchus) likewise had longer test durations and showed a significantly greater latency in reaching for food items than wild- caught females (Cordeiro de Sousa et al., 2001). One other study (Jones et al., 2011b) found

82 that captive-born striped mice were more ‘perseverative’, i.e. prone to the inappropriate repetition of an activity without an appropriate stimulus or function (Sandson and Albert, 1984, Hotz and Helmestabrooks, 1995), than wild-caught individuals. The captive-born rodents entered arms of a radial maze in a more predictable, repetitive way (an effect that helped predict their higher levels of stereotypic behaviour, an issue we review below); although another study found no differences in behavioural flexibility in a radial arm maze between wild-caught and captive-born meadow voles (Microtus pennsylvanicus) (Teskey et al., 1998).

Several additional studies have investigated the impacts of birth origin on handedness as part of research into cognitive development in primates. In chimpanzees, captive-born mother-reared individuals showed significantly stronger right-handed preference than wild- caught conpecifics (Hopkins et al., 2003). Individual gentle lemurs (Hapalemur griseus) also show handedness lateralization, but in contrast there were no significant differences in handedness between the captive-born and wild-caught populations8 (Stafford et al., 1993). Similarly, there were no population level effects of birth origin on handedness in common marmosets (Lopes et al., 2000, Cordeiro de Sousa et al., 2001).

Numerous studies found that captive-bred individuals had impaired cognitive performance compared with wild-caught conspecifics, although several studies found no difference. Additionally, the one study examining brain size found that captive-bred individuals had smaller brains, but the evidence was inconclusive regarding birth/hatch origin effects for perseveration.

6) Abnormal Behaviour e.g. Stereotypies

Numerous studies have examined birth/hatch origin effects in relation to stereotypic and other abnormal behaviours. This section will be organized according to taxon, and then within taxa progress from poorest to strongest evidence. This is because there has been extensive discussion regarding the differing forms that stereotypic behaviour commonly take for different taxa (e.g. pacing in carnivores and oral forms in ungulates) (Mason and Rushen, 2006), and this organization will prevent taxon-specific origin effects from being obscured. Starting with birds, starlings that were captured as juveniles showed more route-tracing and somersaulting than starlings captured and brought into captivity as nestlings (Feenders and Bateson, 2012), and

8 Analyzed from data presented in paper [x2 (1, N = 12) = 0.171, p <0.6788]

83 these behaviours were thought to be linked to increased escape motivation in these birds, as also shown by decreased latencies to move and greater use of the cage walls when in small, confined spaces. Likewise, wild-caught blue jays spent more time route-tracing than hand- reared birds, but were less prone to stereotypic spot-pecking than the hand-reared animals (Keiper, 1969).

Moving on to primates, no differences were found in stereotypic behaviour between wild- caught and captive-born red-capped mangabeys (Reamer et al., 2010). In another study, wild- caught gorillas showed more regurgitation and re-ingestion of food than captive-born conspecifics (Gould and Bres, 1986). In both of these studies, however, wild-caught animals were brought into captivity as very young infants, reared in captivity, and thus were prematurely separated from their mothers. Indeed in the gorilla study, the apparent difference between wild- caught and captive-born individuals disappeared when captive-born hand-raised individuals were compared with the wild-caught captive-reared subjects. In laboratory situations involving chimpanzees and rhesus monkeys, wild-caught individuals were less stereotypic than captive- born animals (Davenport and Menzel, 1963, Mason and Green, 1962); however, in both of these cases the captive-born individuals were taken from their mothers as infants and either hand-reared or put into social isolation (Davenport and Menzel, 1963, Mason and Green, 1962).

Nevertheless, other primate studies show that even when captive-born individuals were not maternally-deprived or socially-isolated, generally they showed more stereotypic behaviours and ‘faeces-smearing’ than their wild-caught conspecifics. In wild-caught macaques (Macaca mulatta and Macaca silenus) stereotypic behaviours were thus absent (Mallapur et al., 2005, Mason and Green, 1962, Berkson, 1968, Wesseling et al., 1988) or greatly reduced (seen in less than 2% of individuals) (Wesseling et al., 1988), in contrast to their zoo- and laboratory- born conspecifics. Furthermore, wild-caught rhesus monkeys engaged in fewer stereotypic behaviours, and fewer other abnormal behaviours such as self-directed biting, than their laboratory-born conspecifics, although these differences were not analyzed statistically (Paulk et al., 1977). In contrast, coprophagia was more prevalent in wild-caught than captive-born gorillas (Akers and Schildkraut, 1985), though it is unknown if this difference was statistically significant. In contrast, Birkett et al (2011) found no difference in abnormal or stereotypic behaviour between wild-born and captive-born chimpanzees.

Looking at studies examining rodents, it was found that wild-caught black rats (Rattus rattus), deer mice (Peromyscus leucopus), bank voles, and African striped mice typically show

84 negligible stereotypic behaviours in laboratory cages, unless caught and caged when very young, even though these stereotypic behaviours emerged rapidly in most of their cage-born offspring (Cooper and Nicol, 1996, Callard et al., 2000, Jones et al., 2011b, Schoenecker et al., 2000, Lacy et al., 2013, Schoenecker, 2009). In contrast, there were no differences in polydispsia (excessive drinking) between wild-caught and captive-bred bank voles (Schoenecker et al., 2000); although in this case it is unknown whether the polydispia was a stereotypic behaviour, or reflected increased needs for water as a result of diabetes (Schoenecker et al., 2000).

In ungulates, zoo keepers have scored zoo-born black rhinoceroses as more stereotypic than wild-caught animals (K. Carlstead, Hawaii, personal communication to Georgia Mason, 2004). By contrast, wild-caught giraffes and okapis (Okapia johnstoni) tended towards more pacing in captivity than captive-born individuals, but showed no differences in oral stereotypic behaviours (Bashaw et al., 2001), although in this report the sample size for wild-caught animals was very small (N< 6).

For carnivores, pacing behaviours were found in only one quarter of wild-caught beech martens (Martes foina) but were present in all of their captive-born offspring (Hansen, 1992). Hansen (1992) also reported that abnormal fur-chewing was absent in wild-caught animals but common in farm-born martens. Studies of polar bears (Ursus maritumus) and other ursids, in contrast, detected no notable differences in stereotypic behaviours between wild-caught and captive-born individuals (Shepherdson et al., 2013, van Keulen-Kromhout, 1978, Ames, 2000), although it is likely that a large number of wild-caught polar bears are brought into captivity as orphans and hand-raised.

Overall there is no clear cut relationship between stereotypic behaviour and birth/hatch origin. However, if only well-controlled studies are examined, where factors such as age of capture and age of maternal separation are taken into account and controlled for, it appears that being wild-caught (especially if not only born but also raised for a period of time in the wild) protects against the development of most stereotypic behaviour. Being wild-caught, in contrast, may sometimes promote certain forms of stereotypic behaviours, such as route-tracing that appears related to escape attempts (e.g. in birds).

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7) Morbidity and Mortality a) Health and disease

When wild-caught and captive-born Iberian lynx (Lynx pardinus) were compared, captive-born lynx were found less likely to be infected with Toxoplasma gondii (Garcia-Bocanegra et al., 2010). In a survey of pet reptiles a higher incidence of intestinal parasites was also found in wild-caught subjects9 (Papini et al., 2011). When the causes of mortality were examined across 16 species of varanid lizards at the Bronx Zoo, results were mixed: captive-hatched varanid lizards had no nematode or fungal infections, but higher rates of both protozoal infections and hemipenal prolapse10 (when the male reproductive organ remains outside the body) (Mendyk et al., 2013).

Many other studies have also found indications that wild-caught individuals may have poorer health in certain respects. A health assessment of captive working elephants in India showed that wild-caught animals had poorer skin condition (Ramanathan and Mallapur, 2008), and dermatoses were likewise more common in wild-caught reptiles than captive-hatched (Harkewicz, 2001). As well, wild-caught owl monkeys showed a trend towards higher levels of creatine kinase suggesting the presence of myocardial infarctions (Gozalo et al., 2008). However, one study found no differences in polydipsia, hypothesized to be a sign of diabetes, between wild-caught and captive-bred bank voles (Schoenecker et al., 2000). Additionally, other studies found indicators of more compromised health in captive-born populations. As previously discussed (see above, ‘Reproductive disorders and physiology’), captive-hatched varanid lizards had much higher instances of reproductive disorders compared to wild-caught individuals (Mendyk et al., 2013). Further, a significant portion of captive-born bank voles were prone to handling-induced seizures even though these were absent in their wild-caught parents (Schonecker, 2009). Finally, during carnivore reintroductions captive-bred carnivores were more susceptible to disease in the wild than their wild-born conspecifics that had been relocated (Jule et al., 2008).

Overall, there appears to be species variability on whether captive- or wild-bred individuals are more susceptible to detrimental health conditions. It often appears, however, that in captivity, diseases relating to infectious agents may be more common in wild-caught animals, but those relating to organ function may be more common in captive-bred animals.

9 This study did not statistically control for phylogenetic relatedness 10 This study did not statistically control for phylogenetic relatedness

86 b) Survival in captivity

Several studies have examined differences in survival and lifespan between wild- and captive- bred or reared populations. In zoos, wild-caught squirrel monkeys appear to have lower survival than their captive-born offspring, but there was no statistical analysis in this study (Zimbler- Delorenzo and Dobson, 2011). One study of fruit flies found that even when genetic differences were controlled for (Carey et al., 2008), the average lifespan of wild-caught fruit flies significantly exceeded that of captive-reared individuals derived from field-collected pupae (Carey et al., 2008). Similarly, in European zoos captive-born Asian elephants had decreased survivorship compared to wild-caught individuals, and this was true regardless of how young they were when entering captivity (Clubb et al., 2008, Clubb et al., 2009). In contrast, wild-caught Asian elephants in the Myanmar timber camps had reduced adult survivorship, perhaps reflecting traumatic methods of capture and ‘taming’ (Mar, 2007, Clubb et al., 2008). Finally, a large-scale analysis of data in the International Species Inventory System (www.isis.org) examined data from 42 species and did not find significant effects of birth origin on longevity for apes, small primates, carnivores, hoofstock, kangaroos, crocodilians, ratites, or raptors11 (Kohler et al., 2006).

The available studies thus reveal some birth origin effects on survivorship in captivity, but no consistent pattern for whether captive-bred or wild-bred populations have increased mortality; although for the better-controlled and more rigorous studies wild-caught individuals appear to live longer.

c) Survival in the wild

Several studies have compared the survival of released captive-bred or reared individuals with native conspecifics in situ. In piping plovers, survival was significantly lower for wild-hatched individuals reared in captivity and later released, than for their wild conspecifics (Goossen et al., 2011). In contrast there was no difference in survival between wild and captive-hatched lacertid lizards (Psammodromus algirus) (Santos et al., 2009). Captive-reared snowy plovers hatched from wild-laid eggs likewise had similar survival compared to native wild-hatched conspecifics (Neuman et al., 2014).

11 This study did not statistically control for phylogenetic relatedness

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In other studies, captive-bred populations were compared with wild-bred individuals that were also released or translocated. For grey partridges (Perdix perdix) survival was lower for captive-hatched individuals released as adults compared with captive-hatched chicks fostered to wild pairs and reared in the wild (Buner and Schaub, 2008). Survival rates of reintroduced timber rattlesnake were lower for individuals hatched and reared in captivity than wild-hatched individuals brought into captivity as neonates to be reared there prior to release (Brown et al., 2007). Similarly, reintroduced captive-born Carnivora had lower survival rates than translocated conspecifics (Jule et al., 2008). In contrast, although captive-born Vancouver island marmots had reduced survival rates during reintroductions than the native wild-born population, captive- born individuals had similar survival to translocated wild-born individuals (Aaltonen et al., 2009). A recent review of 199 reintroduction projects (48% were on mammals, 41% were on birds) found that mortality rates were generally similar between captive and wild-bred individuals (although statistical analyses were not performed), but the causes of mortality differed, with captive-bred individuals being more susceptible to predation and rates as ‘less able to cope’12 (Harrington et al., 2013): a pattern consistent with our findings in the previous ‘Anti-predator behaviour’ section.

In general, where there were effects of birth/hatch origin, reintroduced captive-reared individuals showed reduced survival compared to the wild-born populations.

Discussion

To summarize the main results of this literature search and review, there was evidence that natural behaviours were compromised or different in captive-bred individuals, and not surprisingly, these individuals sometimes had increased mortality and were generally rated as ‘less able to cope’ when released into the wild compared to wild-bred conspecifics. Captive- bred individuals were sometimes larger and more obese, and there was some evidence they reproduced earlier. In the few instances where this was studied, captive-bred individuals were also generally found to have impaired cognitive performance and possibly smaller brains (though only one study examined this). Consistent with this result, focusing on high quality studies, captive-bred individuals appear to be more susceptible to developing most stereotypic

12 This study did not statistically control for phylogenetic relatedness

88 behaviours in captivity and are therefore more perseverative. Wild-caught individuals in contrast exhibited greater indications of stress and fear of humans and anthropogenic stimuli in captivity and escape-related stereotypic behaviour. Yet, despite this, were often more fertile and reproduced more successfully in captivity, and generally showed better parental care and had greater infant survival (although, in some cases, higher incidences of infanticide). Wild- bred males also often seemed more competitive and/or attractive than their captive-bred conspecifics. In terms of health, wild-caught individuals may be more prone to infectious disease, and less susceptible to developing disease related to organ function. The relationship between birth origin and longevity in captivity is unclear and varies across species; however, the more rigorous studies with better controls suggest that wild-caught individuals may live longer in captivity. A caveat for the results of this review is that for many birth/hatch origin effects few studies have been conducted, so it is difficult to conclusively determine the effects with confidence; thus these are tentative conclusions.

This literature review thus found numerous birth/hatch origin effects, even when potential confounds such as genetic and environmental differences were controlled for. A key distinction important for interpreting and understanding these birth/hatch origin effects is whether they reflect adaptive, maladaptive, or malfunctional changes. Adaptive changes are normal expressions of phenotypic variation that can help the individual to cope with the current or adult environment, sometimes known as ‘experience adaptive effects’ (Greenough et al., 1987), and they are relevant when we examine captive-bred animals living in captivity and wild-bred animals living in the wild. For example, captive-bred animals often show domestication-like effects within a single generation (Mason et al., 2013). In this review too, captive-bred individuals were often found to exhibit numerous traits which are adaptive for the captive environment (e.g. being bolder and less fearful of humans). Maladaptive traits, in contrast, are those which are adaptive in one environment (e.g. the developmental one) but ill-suited for the current environment; these can thus occur when an organism finds itself in an environment at odds with the adaptive plan developed for another one (Rutter and O'Connor, 2004). This is often illustrated by the effects seen when captive-bred animals are moved to the wild, and wild- bred animals are moved to captivity. Maladaptive traits were exhibited by both wild-caught individuals in captivity (e.g. high levels of fear to stimuli, such as of humans, and elevated cortisteroid levels levels), and by captive-bred individuals released into the wild (e.g. in their loss of foraging, anti-predator, and sheltering behaviours). Finally, malfunctional traits represent true pathology and are not beneficial in any environment (Mills, 2003). Captive-bred individuals

89 were found to have numerous malfunctional traits in captivity (e.g. obesity, reproductive failure, stereotypic behaviour, seizures). It is also possible that malfunctional traits played a role in the difficulty coping and excessive mortality sometimes observed when captive-bred individuals were released into the wild. In contrast, malfunctional traits appear to not be found in wild-bred individuals.

Genetic differences between captive-bred and wild-caught populations were minimized in this review by comparing wild-caught individuals with F1 captive-bred individuals. However, similar to the discussion regarding the age of transfer to a new environment, this criterion will not have eliminated genetic differences between wild- and captive-bred animals entirely: wild- caught individuals which successfully breed in captivity and their offspring that survive to adulthood may represent a non-random sample of the population, a process referred to as ‘winnowing’, which would lead to genetic differences between wild-caught and F1 populations in captivity as well as released captive-bred and F1 populations in the wild (Morton, 1991, Spurway, 1955). Supporting this, numerous studies have found evidence suggesting that the genetic selection of a population for the captive environment can occur very rapidly, sometimes even with only one generation of captive breeding (Salonen and Peuhkuri, 2004, Ellner et al., 2011). Christie et al (2012), for example, found that the first generation of captive-bred steelhead trout in a hatchery had substantially greater reproductive success then wild-hatched conspecifics, and furthermore, that for the wild-hatched conspecifics those that reproduced better in captivity produced offspring that faired worse in the wild. The effect of winnowing and genetic selection between populations would be to increase the magnitude of birth origin effects, since the captive-bred population, for example, would thence exhibit rapid adaptation to captivity due to both phenotypic plasticity and genetic changes. Another potential confound is that although all effects known to be rapidly and completely reversible were excluded, given enough time in the new environment, it could well be more of the these noted origin effects may also prove reversible (e.g. effects on health and on body fat). The effect of this confound would again be to increase the perceived magnitude of these birth/hatch origin effects. A final confound is that many individuals did not neatly fall into the definition of being fully captive or wild-bred (i.e. beginning life and then being reared in each respective environment); thus the developmental stage at which an individual was transferred from the wild to captivity (or vice versa) had to be taken into account when classifying the birth origin of these individuals for the purpose of this review. While these efforts lessened the impact of including these cases, the

90 overall effect of including them would be to minimizing the origin effects since they had experience during early development in both the captive and wild environments.

Possible Mechanisms Underlying Birth/Hatch Origin Effects

Nutrition in captivity

Some of the observed effects detected when comparing captive-bred and wild-bred individuals in captivity may result from increased access to food resources. Captive-bred individuals have access to these extra resources their entire lives, including at critical developmental stages, while wild-caught individuals do so for only a portion of their lives. Thus for example, De Vleeschouwer et al. (2003) hypothesized that captive-born female lemurs had larger litters than wild-caught mothers as a result of their life-long improved nutritional status, with wild-caught mothers remaining at a disadvantage when captive due to some inability to channel the extra resources into reproductive output.

While the abundance of food in captivity likely reduces problems with under-nutrition, it may well lead to obesity and its adverse consequences (e.g. cardiovascular disease, cancer, diabetes, decreased fertility and shortened lifespan), as was suggested regarding zoo-born elephants and their calves (Clubb et al., 2009). Furthermore, while captive populations often have access to more abundant food, it is not necessarily nutritionally superior and may not be as variable or species-appropriate as a wild diet. This will depend on how closely management is able to replicate and source components of a wild diet. For example, captive carnivores are often fed a ground meat diet rather than whole carcasses, which has been associated with dental disease (Fagan, 1980a, Fagan, 1980b, Vosburgh et al., 1982, Haberstroh et al., 1984), and morphological changes of the jaw, skull, and teeth (O'Regan and Kitchener, 2005, Duckler, 1998). Additionally, giraffes in captivity often eat pelleted feed and hay (grass) rather than the strict diet of browse (leaves) found in the wild (Clauss et al., 2007). This captive diet is more abrasive than the wild diet, and it is thought to be linked to increased teeth wear and early death associated with extreme fat atrophy (Clauss et al., 2007), and may help explain why, although captivity is generally more resource abundant, captive-bred individuals do not always have optimal health or physical well-being. Differences between captive and wild diets may thus underlie certain birth origin effects relating to health, longevity, morphology, reproduction, and foraging behaviour. It is therefore also unsurprising that many studies have found that

91 captive-bred animals are larger/heavier than wild animals in the wild (Clubb et al., 2009, Terranova and Coffman, 1997, Courts, 1999, Whitten and Turner, 2008) .

Such nutritional effects suggest that for some changes, the longer that captive-bred and wild-bred animals share a similar captive environment, the more likely they are to converge to identical well-conditioned phenotypes; and the longer that captive-bred and wild-bred animals share a wild environment, the more likely they are to develop indistinguishably lean phenotypes. Thus, for differences in body mass and body fat, any birth/hatch origin effects may wear off when previously differentially-fed and exercised animals come to share the energy balance. The one exception could be if a nutritionally deprived rearing environment has a lasting effect by programming a 'thrifty phenotype' (Hales and Barker, 2013), which has been associated with obesity in adulthood (Ravelli et al., 1999, Rhodes et al., 2009). This predicts that infants born to lean wild-bred mothers (regardless of whether in the wild or in the captivity) would, if then raised in the resource-rich conditions of captivity, be predisposed to obesity compared to captive-bred animals who have been gestated and raised in these conditions of plenty: an interesting hypothesis for future test.

Veterinary care

In captivity animals typically also have access to another valuable resource: regular veterinary care, including treatment of disease and injuries, inoculations, and other preventative measures such as parasitides. Captive-bred animals will have received such medical treatments for their entire lives, while their wild-bred peers would have only had access since entering captivity. This is likely to explain why wild-caught animals often have more infectious conditions. Like nutrition, the benefits of medical care might accrue with time (and unlike nutrition, not have any specific sensitive periods). Therefore, after long enough periods of time with medical care in captivity, or long enough without it in the wild, captive-bred and wild-bred individuals should come to converge minimizing the population differences. However, unlike receiving an overabundance of food, getting good health care is unlikely to ‘backfire’ and cause problems (unless there were long-term side effects associated with certain medical treatments, or too much hygiene were to increase allergies and autoimmune issues, as speculated for humans; e.g. Okada et al., 2010).

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Stress, fear and their functional consequences

Evidence was found suggesting that wild-caught individuals have increased corticosteroid levels, increased stereotypic behaviour resembling escape attempts (in birds), and decreased activity in captivity, which suggests that they experience high levels of stress and fear in captivity. This makes sense considering that wild-caught individuals in captivity will be regularly exposed to novel stimuli, especially humans, which they did not have an opportunity to experience and habituate to during early development. The relative lack of fear of humans and other anthropogenic stimuli typical of captive-bred individuals is adaptive in the captive environment because these animals are not chronically stressed and do not expend their energy on unnecessary escape attempts and avoidance behaviours. When wild-bred animals in captivity fear humans it is clearly maladaptive; this fear would have been beneficial in the wild since humans are often a genuine threat to the survival of wild animals (e.g. poaching, Mfunda and Roskaft, 2010, regulated hunting, Cousineau et al., 2014, pest control, Baldwin et al., 2014), but creates a state of chronic fear and stress in captivity.

Interestingly, when wild-bred individuals were exposed to predators during development this led to an increase in fear, while when captive-bred individuals were exposed to humans during development this resulted in decreased fear. This suggests that learning may well be involved in forming these differential responses. When predator cues in the wild are followed by indications of danger, such as conspecific warning signals, animals will often increase their response to predator cues (Griffin, 2004, Whittaker and Knight, 1998). This would occur through the process associative learning, whereby an association between a stimulus and an event is learned (Manning and Dawkins, 1998). For example, in black-tailed prairie dogs (Cynomys ludovicianus), alarm calls paired with predator exposure increased anti-predator behaviours and had lasting effects which improved reintroduction survival (Shier and Owings, 2006). Captive-bred animals released into the wild may thus eventually become as wary as wild-bred conspecifics, if they survive long enough. In contrast, in captivity the presence of humans will frequently not be followed by harm to the individual (the exceptions may include medical procedures), and often will proceed the delivery of food. The lack of fear towards humans in captive-bred animals may thus involve: associative learning; habituation, ‘a waning of response to a repeated, neutral stimuli’ (Whittaker and Knight, 1998); and/or socialization, which is the process where a long-term familiarity with stimuli is developed, allowing for proper species-identification and avoidance of novel stimuli later in life (Lord, 2013). Of these three processes, those of habituation and associative learning would predict that captive-bred and

93 wild-bred animals should converge the longer they share a common environment, since they reflect reversible effects that should track current experience. Socialization in contrast has a sensitive period: it only occurs in young animals, and its effects are then long lasting and hard to reverse (e.g. Lord, 2013, Scott et al., 1974). Socialization effects would predict that if captive- bred and wild-bred individuals had differential human contact during their sensitive period for socialization, these differences in how humans are reacted to should remain for life. However, another reason why birth/hatch origin effects may not always be seen is that some reactions to predator cues are genetically preprogrammed and instinctive (e.g. Jesuthasan and Mathuru, 2008). This therefore might also explain cases where there were no birth/hatch origin effects for anti-predator responses.

When comparing wild-bred and captive-bred animals that are currently in the same environment, one population has typically experienced a more extensive capture and transportation process, and this may be another reason for differential stress. Wild-caught animals brought into captivity may be chased, trapped or netted, confined during transportation, and possibly even smuggled or traded on the black market; for example, African grey parrots (Psittacus erithacus) are often injured during capture and during transport they may endure harmful conditions including rough handling and inappropriate storage (Schmid et al., 2006). Capture and transportation have a negative impact; for example, wild-caught Asian elephants in Burmese timber camps had compromised longevity as a result of the capture and taming process (Clubb et al., 2008, K., 2007). As we have seen, many studies looking at the reintroduction of captive-bred animals into the wild control for this by releasing wild-bred individuals for comparison; this allows effects of birth origin to be separated from effects of relocation stress. When capture and transportation stress are not properly controlled for, the likely result would be an exaggeration of apparent birth origin effects since the transported population is exposed to additional stressors. Such birth/hatch origin effects of capture and transport stress may be reversible, depending on the degree of trauma experienced or whether it occurred during a crucial sensitive period.

‘Negative-contrast’ effects, where a current circumstance is perceived as being more negative due to a comparison with a more favorable previous circumstances (Zeaman, 1949), may also underlie some differences in stress between captive-bred and wild-bred individuals. Wild-caught individuals may perceive specific aspects of the captive environment as being more negative than captive-bred individuals due to their previous experiences, leading to greater frustration. For example, in captivity, as I have reviewed, there is less space, minimal

94 opportunity to perform natural foraging, and less ability to make choices (such as choosing social grouping, movement and ranging patterns, or to approach or retreat from stimuli). Negative-contrast paradigms often result in elevated corticosteroid output, increased behavioural activation (specifically attempts to escape or perform thwarted behaviours), followed by inactivity when these behaviours extinguish (reviewed by Latham and Mason, 2010). It is likely that expectations would be learnt and unlearnt throughout the lifetime of an individual. Thus one might expect the elevated frustrations of wild-bred animals in captivity to wane with time, and this would result in the disappearance of the birth/hatch origin effects to decrease with time in captivity.

Stress and fear may also contribute to the birth/hatch origin effects found for infant mortality. In numerous studies it was found that wild-caught individuals had better parental care, with less infanticide and higher infant survival, than captive-bred individuals (although, several cases were found where the opposite was true). Studies show that individual differences in stress responses are related to infanticide tendencies. For instance, in silver foxes (Vulpes vulpes), females who committed infanticide had faster responses to stressful stimuli (Bakken et al., 1999). Schmalz-Peixoto (2003) suggested that wild-caught dams may commit more active infanticide than captive-bred dams because they perceive the environment as being more inadequate or are more stressed. Having stressed, wild-caught parents may also have a detrimental impact, leading to offspring differences between wild- and captive-bred populations. For elephants it has thus been hypothesized that if the dams are stressed this may increase stress in their offspring, leading to detrimental effects on survivorship (Clubb et al., 2009). However, all these hypotheses still await proper testing.

Differences in stress and fear between captive-bred and wild-bred individuals may also explain a number of other birth/hatch origin effects. Wild-caught individuals may be more susceptible to certain health conditions due to increased stress and fear. Stress can lead to compromised immune function and increased susceptibility to infectious agents, and other health conditions such as cardiovascular disease and autoimmune conditions (Segerstrom and Miller, 2004, Zorrilla et al., 2001, Schneiderman et al., 2005). When captive-bred individuals are released into the wild they are likely to be more stressed than their wild conspecifics, thus leading to the increased susceptibility to disease, altered activity levels and behaviour, and reduced survival and coping ability discussed above.

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Environmental complexity and its effects on brain and behavioural development

Differences in environmental complexity may also underlie some of the observed birth/hatch origin effects. The wild environment is typically more complex (e.g. with more variability, novelty, and unpredictability) than captive environments. Extensive research has shown that environmental complexity during development increases brain size, cognitive abilities and forebrain function (e.g. Marshall and Kenney, 2009, Burns et al., 2009, Kihslinger and Nevitt, 2006, van Dellen et al., 2000, Falkenberg et al., 1992). Thus much of the work studying the effects of environmental enrichment has found that complex, naturalistic early environments produce more normal brains with better abilities to learn new tasks and greater behavioural flexibility (e.g. Rosenzweig and Bennett, 1996, van Praag et al., 2000, Sale et al., 2014, Bell et al., 2009). Exposure to more complex wild environments during development may therefore explain why wild-caught individuals generally have improved cognitive abilities and possibly larger brains compared to captive-bred conspecifics. In this review, admittedly only one paper found a difference in brain size between captive-bred and wild-caught populations. However, several authors have found that captive-bred lions and tigers have smaller cranial volume in comparison to their free-living wild conspecifics and have suggest that experience rather than genetics may underlie these differences, although this was not explicitly tested (Saragusty et al., 2014, Yamaguchi et al., 2009). If true, this would predict captive-bred lions and tigers would have smaller brains and crania than their wild-caught conspecifics, particularly those caught in adulthood. The few studies examining whether there are sensitive periods regarding brain structure and function have surprisingly found that exposure to a complex environment reaps benefits over a variety of ages (Rosenzweig and Bennett, 1996, Kempermann et al., 2002). More research is needed to clarify the extent that individuals deprived of complexity in early life are able to catch-up in terms of brain structure and function.

Small-brained phenotypes may be adaptive when captive-bred animals are in captivity; brain tissue is energetically expensive to maintain (Aiello and Wheeler, 1995, Kotrschal et al., 2013) so large-brained phenotypes only make sense when the benefits of increased cognitive abilities outweigh the energetic costs (Gonda et al., 2013, Kotrschal et al. , 2013). However, when captive-bred individuals are released into the wild these phenotypes would be maladaptive, since cognitive abilities likely influence navigation, foraging abilities, social behaviour, including reproduction, and many other natural behaviours crucial for fitness. Death may also occur before the captive-bred animals are able to catch-up and improve these skills. Impaired cognitive abilities as a result of developing in captivity may be another mechanism

96 underlying the increased mortality and decreased ability to ‘cope’ sometimes seen when captive-bred individuals are released into the wild. In specific circumstances the phenotype of the captive-bred individuals may even be malfunctional. For example, the seizure activity noted for captive-born bank voles may reflect CNS dysfunction; environmental enrichment has been shown to decrease seizure activity in mice (Manno et al., 2011, Young et al., 1999, Auvergne et al., 2002), suggesting that in the case of the bank voles the barren captive environment experienced during development may have led to a predisposition for seizure activity, which is malfunctional for the individual.

Another malfunctional trait is stereotypic behaviour resulting from altered basal ganglia function; as discussed by Lewis et al. (2006) stereotypic behaviour, “is characterized by strikingly periodic, predictable or regular dynamics …representing a loss of complexity associated with CNS insult.” Environments lacking complexity are thus known to affect cortical- basal ganglia loops in the forebrain, leading to abnormalities in behavioural disinhibition, and predisposing individuals to stereotypic behaviour (Garner, 2006, Lewis et al., 2006, Garner, 2005). Although the evidence is not clear in all cases, it appears that being captive-bred may also be a risk factor for developing stereotypic behaviour. Thus these forebrain changes may underlie the development of stereotypic behaviour in these individuals. Exposure to such barren or confined captive environments early in life may be more impactful (Jones et al., 2011b, Odberg, 1987, Berkson, 1968), suggesting that there is a sensitive period early in development (although there are cases where enrichment later in life can reduce stereotypic behaviour; Odberg, 1987, Meehan et al., 2004). This may explain why at older age at capture predicted more protection from developing this behavour in wild-caught African striped mice (Jones et al., 2011a).

Finally, complex, naturalistic developmental environments also provide specific experiences that allow for the mastery of particular natural skills. Thus in addition to hindering general brain development and cognitive abilities, captive environments lacking complexity provide limited opportunities for individuals to learn the physical coordination and dexterity required for certain locomotor and foraging skills, as well as social, reproductive, and other forms of natural behaviour. This may slow down and prevent the learning of specific skills and behaviours, as was found to be the case for many captive-bred animals. For some such forms of learning, it seems individuals are often more proficient when the skills or behaviours are learned young, but even adults can continue to learn and improve upon their skills. For example, in black rats a higher percentage of pups learned pine-cone stripping techniques when

97 exposed to pine cones from birth, versus at 20 days old (Zohar and Terkel, 1996). Further, for captive-bred golden lion tamarins released into the wild, locomotor abilities improved during the first 6-18 month for all individuals, but the greatest changes were observed in adolescents compared with adults (Stoinski and Beck, 2004). In other cases it appears certain behaviours or skills do have set sensitive periods earlier in development, and the correct type of experience during these time frames is very important for normal behavioural development. For example in many species this is true for learning the characteristics of potential mates (Kendrick et al., 1998, Kozak and Boughman, 2009, Horwich, 1989, ten Cate et al., 2006), social group members (Kendrick et al. , 1998, Schusterman et al., 1992, e.g. Dyer et al., 1989), and the hatch location so that individuals can later navigate back (Putman et al., 2014, Lohmann et al., 2013). These birth/hatch origin effects regarding the development of specific behaviours and skills will be either adaptive (for captive-bred individuals living in captivity, or wild-bred animals living in the wild), or maladaptive (for captive-bred animals moved to the wild, or wild-bred subjects moved to captivity); however they will not be malfunctional since they represent individuals developing skills and behaviours that are appropriately suited for their rearing environment.

Physical effects of experience

Physical morphology can also remodel according to experience. Several fish studies identified morphological differences in the shape and relative size of the fins and body between the captive- and wild-bred populations; and these differences cannot be easily explained by any of the previously mentioned mechanisms. One possible explanation is that the differing experiences between the populations led to altered morphological development. This is a hypothesis that has been discussed for other species. For example, changes in leg bone length and body size of black-footed ferrets (Mustela nigripes) (Wisely et al., 2005), and structural differences in jaw and skull morphology between captive and wild tigers (Duckler, 1998) have been attributed to different activity patterns leading to divergent morphological phenotypes. However, in each of these cases it was unknown if the differences truly resulted from different birth and rearing environments, or if there were confounding issues involved, such as genetic differences, that may have been responsible for the reported effects. Additionally, as previously discussed experience has been shown to alter the gut-length in birds (see ‘Introduction’), and this rapidly reverses once the individual is switched between the captive and

98 wild environments. It appears that physical morphology may have sensitive periods for some traits, particularly those involving bone or cartilage such as in the ferret and tiger examples, but may be highly plastic for other traits, such as for gut length in birds. Similar to other birth origin effects, these changes are possibly adaptive for animals that stay in their rearing environment, but possibly maladaptive if they switch from captivity to the wild, or vice versa.

Practical Implications and Future Research

When there is a mismatch between rearing and current environments, it may cause harm and stress to those individuals, with great ethical implications. The accumulated evidence that wild- caught animals in captivity are more stressed and captive-bred animals in the wild have more difficulty coping with the wild environment, suggests these populations are more likely to have poorer welfare. This has ethical implications in a number of educational, conservation and economic areas. Wild animals have commonly been brought into captivity for laboratory research (e.g. Feenders et al., 2011, Burns et al., 2009, Hansen, 1992), for endangered species captive-breeding programs (e.g. Keeley et al., 2012, Roche et al., 2008), and to supply the demand for wild-caught specimens and hard-to-breed species in the exotic pet and aquarium industries. Although zoos are working to phase out the collection of specimens from the wild (WAZA 2005, IUCN 1993), due to ongoing issues such as climate change and rapid extinction it is likely that intensive conservation management approaches will be needed (Minteer and Collins, 2013) that involve bringing wild individuals into captive and semi-wild contexts (see Chapter 5 for further discussion). As discussed above, there has been much speculation about the welfare of such wild-caught animals in captivity. The mismatch between wild environments inhabited by these subjects during development and their current captive environment results in individuals with poor abilities to cope with or adapt to captivity. This confirms the good judgment of recent legislation passed by the European Union banning the use of wild-caught animals in laboratory research. Additionally, differences between wild- and captive-bred animals have been well-documented in terms of behaviour and skills necessary for survival in the wild and are sometimes less successful when reintroduced into the wild then wild-bred conspecifics. Thus, in this case too, the ethical implications of moving animals from their rearing environment to a novel environment should be carefully considered. The use of environmental enrichment to mimic wild-rearing (Biggins et al., 1999, Stoinski et al., 2003), and to off-set or modulate the

99 effects of captive-rearing and encourage wild behaviour (Shyne, 2006, Swaisgood and Shepherdson, 2005) should be continued.

Beyond ethical considerations, the birth origin of study subjects can be relevant when designing scientific studies. The findings of this review indicate that captive-bred individuals may be inappropriate models for normal cognitive, behavioural, and reproductive processes due to the evidence of malfunctional traits in these areas (and additional malfunctional traits may become apparent as further evidence accumulates). Even when the differences between wild- and captive-bred individuals are due to adaptive or maladaptive traits and not malfunction, any systematic differences between these populations would make captive-bred individuals inappropriate models for wild populations, an issue that is rarely addressed (Meagher et al., 2012). However, captive-bred individuals may be accurate models for some phenomena, such as diseases of the Western world, particularly those related to obesity. In addition, comparing well-nourished captive-bred populations with more deprived wild-bred populations would be good for studying population and genetic differences in ‘thrifty phenotypes’. Furthermore, Mason et al (2013) suggested using wild-bred animals brought into captivity as a model for ‘human induced rapid environmental change’ (HIREC), such as deforestation or urbanization, since individuals exposed to HIREC in the wild will experience many circumstances analogous to wild-caught animals exposed to captivity, such as novel habitats, altered inter- and intra- species interactions, disrupted physiological process due to changes in climate, humidity, and other environmental factors. Studying birth origin effects could thus give insight into the magnitude of relevant plasticity within a population, and the underlying mechanisms could providing invaluable information regarding the processes involved when reacting to HIREC (Mason et al., 2013). Furthermore, it could help illuminate fundamental processes underlying the development of a wide variety of traits, providing valuable information regarding the factors that alter and influence the developmental processes in a particular species. For example, studying birth/hatch origin effects may also help identifying experience-independent aspects of behaviour that reflect strong selection pressures for invariant responses (McNamara and Houston, 2009), for example migratory behaviour (Pulido and Berthold, 2010). The majority of the cross-species studies in this review did not control for phylogeny, future studies examining species comparisons should control for phylogeny so the results are not confounded due to phylogenetic signal (see Chapter 1).

The findings from this review open up many additional avenues for future research into birth/hatch origin effects themselves. Research is needed to better distinguish experiential

100 effects (plasticity) from side-effects of ‘winnowing’ (genetics). It is also important to identify the effects of the timing (e.g. experience during specific sensitive periods) and duration of early experience. For example, Jones et al (2011b) showed that the duration of experience in a wild environment was important for the development of stereotypic behaviour in wild-caught African striped mice, while Clubb et al (2008, 2009) showed it was unimportant for survivorship in wild- caught Asian elephants. Investigating the timing and duration of common and shared experiences once animals with different birth or hatch environments are housed similarly is also important to see how long-lasting or reversible these origin effects are. Efforts to use environmental enrichment to off-set or modulate the effects of captive-rearing and encourage natural behaviour patterns, discussed above, are not always successful (e.g. Burns et al., 2009), and more research is needed to determine how to best reduce the impact of captive- rearing. Overall, due to the large number of potential confounds (see above) when investigating birth/hatch origin effects, there is a great need for studies that are specifically designed to minimize the impact of these confounds.

In summary, numerous differences were found between captive- and wild-bred populations, even with controls for confounding factors such as genetic differences, the age individuals were transferred between environments, and reversible phenotypic changes. Briefly, both captive and wild-bred individuals often exhibit maladaptive traits when living in an environment different from where they were reared. Additionally, captive-bred individuals exhibit numerous adaptations to the captive environment, but also some pathologies which may stem from inadequacies in their rearing environments. Mechanisms underlying these birth/hatch origin effects may include nutrition, veterinary care, the outcomes of stress and fear, differences in the environmental complexity of the rearing environment, as well as physical effects of experience. Due to the large impact birth/hatch origin has on the phenotype of individuals it is thus important to it when making decisions regarding welfare, conservation and the design of sound scientific experiments. More research is needed to better understand the extent of these birth/hatch origin effects, as well the underlying mechanisms.

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Chapter Four Birth Origin as a Risk Factor for Stereotypic Behaviour in Carnivores

Introduction

Chapter 2’s analyses revealed important information regarding species-level risk factors for captivity; however they did not clarify the mechanisms underlying the detrimental effects of captivity. With respect to the development of stereotypic behaviour, three non-mutually exclusive mechanisms have been described: 1) maturing in a constrained captive environment affects forebrain development and functioning; 2) chronic stress affects forebrain functioning; and/or 3) frustrated motivations to perform natural behavioural responses are chronically triggered by the environment (Mason, 2006b). Campbell et al. (2013) reviewed the current literature and found that there is evidence to suggest that in captive animals stereotypic behaviour is a common response to a sub-optimal environment during development, but the evidence was not conclusive regarding the underlying mechanisms. As of yet, no study has systematically investigated these mechanisms across a large number of captive wild species.

As discussed previously (see Chapter 3) research studies examining topics such as environmental enrichment and neurobiology have shown that constrained, impoverished captive conditions during development can lead to CNS dysfunction. Specifically, when the cortical- basal ganglia loops are affected this may lead to abnormalities in behavioural disinhibition and the development of stereotypic behaviour (Lewis et al., 2006). Chronic stress may also lead to stereotypic behaviour through a similar mechanism, where the cortical-basal ganglia loops are affected by the sustained levels of stress, again leading to the development of stereotypic behaviour (Mason, 2006b). Frustrated motivations to engage in specific behaviours in captivity (including natural behaviours, such as hunting, and escape attempts) may lead to sustained attempts to perform these behaviours, eventually developing into stereotypic behaviours that bear a resemblance to these original motivated behaviours (Mason, 2006b, Dixon et al., 2008, Nevison et al., 1999).

In general, captive-bred individuals mature in physical environments that are relatively impoverished and their behaviour is constrained compared to their wild-bred counterparts (see Chapter 3). Furthermore, across many species there is evidence that wild-bred animals may be protected from the development of stereotypic behaviour in captivity (Chapter 3; Latham and Mason, 2008, Mason, 2006a), and the same may be true for animals reared in more enriched

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environments (e.g. African striped mice, Rhabdomys: Jones et al., 2011a). On the other hand, there is evidence that wild-bred individuals taken into captivity may experience greater levels of stress and fear than their captive born/hatched conspecifics (see Chapter 3). Additionally wild- caught individuals may experience stronger frustrated motivations to perform natural behaviours; there is evidence that they experience ‘negative-contrast’ effects in captivity, and for some taxa, elevated escape-related stereotypic behaviour (see Chapter 3). Thus, differences between captive-bred and wild-bred populations may provide a system to differentiate the effects of CNS dysfunction resulting from abnormal development in captive-bred populations, from the effects of relatively increased stress and frustrated motivations experienced by wild- bred populations in captivity, as they relate to the development of stereotypic behaviour.

The main objective of this work was therefore to use the known relationships between stereotypic behaviour and the variables related to species’ wild behavioural biology found in Chapter 2 to investigate the mechanisms underlying the development of carnivore stereotypic behaviour. The first hypothesis is that the high severity of stereotypic behaviour observed in captive carnivore species that are wide-ranging in the wild, and/or those with long chase distances in the wild, is due to changes in the brain resulting from inabilities to develop normally in constrained captive environments. If true, captive-born individuals will show a stronger positive correlation between stereotypic behaviour and these variables for wild behaviour compared to wild-born individuals. The second testable hypothesis is that the high severity of stereotypic behaviour observed in captive wide-ranging and/or long-chasing carnivores is a result of stress or frustration from not being able to express species-typical behaviour patterns. In contrast to the first, this hypothesis predicts that wild-born individuals will show a stronger positive correlation between stereotypic behaviour and these wild behaviour variables compared to captive-born individuals. In addition, examining the remaining wild variables that were not significantly correlated with stereotypic behaviour in Chapter 2 may also be fruitful. If captive and wild-born populations have different susceptibilities to developing stereotypic behaviour, then pooling these populations together may have led to non-significant results (Type II errors). Therefore further investigations examining birth origin and natural history interactions may provide useful insights into the relationships for these variables.

Furthermore, additional hypotheses can be tested by examining birth origin differences between locomotor stereotypic behaviour and all stereotypic behaviours combined. If locomotor stereotypic behaviour is more severe and/or has a stronger correlation in wild-born carnivores, then this would support the hypothesis that stereotypic behaviour results from increased stress,

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fear, and/or frustration in captivity; since pacing could represent thwarted ranging, hunting or escape behaviour. In contrast, if stereotypic behaviour results from CNS dysfunction, then being captive-born should predict all forms of stereotypic behaviour and not just locomotor forms, since CNS dysfunction would predispose individuals to develop a variety of behavioural abnormalities and not just those associated with a specific ecological niche. For example, stereotypic behaviours exhibited by individuals with autism (Lewis and Kim, 2009) and those induced by drug administration (amphetamine or apomorphine) in deer mice (Peromyscus maniculatus bairdii) and rhesus monkeys (Macaca mulatta) (Lewis et al., 1990, Presti et al., 2002) encompassed a larger variety of forms than when performed by the non-autistic children and control animals in these studies. Overall, this work could enhance the fundamental understanding of the mechanisms underlying stereotypic behaviour, providing valuable information that can be used to development appropriate solutions to alleviate or reduce stereotypic behaviour in captive carnivores.

Methods

General Overview

Data on the natural behavioural biology of each species was obtained from the Wild Carnivore Behaviour Database_2010 (see Chapter 2). The updated Captive Carnivore Stereotypic Behaviour Database_2010 (see Chapter 2), containing data for 51 species and more than 1,300 individuals, was used for the birth origin analyses.

Data Collection

As part of the initial literature search, where possible, birth origin and other identifying information such as age and sex were recorded and entered into this database. Birth origin data were, however, absent for more than 85% of individuals in the Captive Carnivore Stereotypic Behaviour Database_2010. The authors of each study that had been entered, and the zoos or institutions which housed the individuals, were therefore contacted to request the missing information. Information requested including birth origin, sex, and the age at which each individual entered captivity (for wild-caught individuals). The survey was very successful, with ~88% of zoos and ~67% of authors responding to provide this additional information.

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Quality control

Rearing history (being mother or hand-reared) is a confounding factor that can obscure birth origin effects (see Chapter 3); thus all individuals known to be hand-reared were excluded from the analyses. However, individuals with unknown rearing history were kept in the database (even though some would have been hand-reared), since if all the individuals with unknown rearing history were excluded the sample size would have been too small.

Wild-born individuals brought into captivity at a young age may resemble captive-born individuals in phenotype as a result of being exposed to captive conditions during critical developmental phases (see Chapter 3); thus the age at which wild-born individuals entered captivity is another confounding factor that needed to be taken into account. Individuals were categorized, wherever possible, according to the life stage they entered captivity, and those that entered captivity prior to their species’ natural dispersal age were excluded from analyses. The average natural dispersal age for each species was obtained from the PanTHERIA database (Jones et al., 2009). For the sun bear (Helarctos malayanus) dispersal age was not available in the PanTHERIA database so this information was obtained by searching the primary literature using the search engine Web of Science (www.webofknowledge.com) for studies examining the timing of developmental milestones in this species. However, individuals for whom the age at which they entered captivity was unknown were included, since otherwise, as before, the sample size would have been too small for statistical analyses. After these quality control procedures, the database contained 33 species with 59 known wild-born and 139 known captive-born individuals.

Calculation of species medians

Similar to Chapter 2, stereotypic behaviour was recorded as the percent of observation time individuals spent engaged in stereotypic behaviour. Study means for stereotypic behaviour were calculated for each birth origin group (wild-born or captive-born) for locomotor and all stereotypic behaviours combined from individual means. Again, only stereotypic individuals were included in the calculation of study means (see Chapter 2). The study means were then used to calculate species medians (so that very high or very low values from some studies were not overly influential, as per Chapter 2). Similar to previous analyses (see Chapter 2) the vast majority of stereotypic behaviours were locomotor. Consequently, species medians for the final

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analyses were calculated for locomotor stereotypic behaviour and all stereotypic behaviours combined, but not oral or stationary stereotypic behaviour on their own. Note that when poorly sampled species involving fewer than five individuals in a group (wild-born or captive-born) were excluded the sample size was too small for any of the statistical tests to run. Thus, medians were calculated even for poorly sampled species and birth-origin sub-groups. Table 1 lists the species medians for stereotypic behaviour for each birth origin, and the number of individuals that had data for each variable. Species medians for the 12 wild behaviour variables were obtained from the Wild Carnivore Behaviour Database_2010 described in Chapter 2.

Confounding factors

As previously discussed, species medians cannot be treated as independent data points since related species will share traits due to a common ancestry, a phenomenon termed phylogenetic inertia (Felsenstein, 1985). To take this into account, as in Chapter 2, phylogenetically independent contrasts (Felsenstein, 1985) were calculated with the PDAP module (Midford et al., 2005) in Mesquite version 2.75 (Maddison and Madison, 2006) using the complete phylogenetic carnivore supertree (Nyakatura and Bininda-Emonds, 2012). Many natural history variables correlate with body mass (Gittleman, 1985); thus the relationship between body mass and the natural behavioural biology variables listed in Table 1 had been investigated in Chapter 2. The variables found to correlate with body mass were controlled for in all analyses by adding body mass to the statistical models as a covariate. Furthermore, the birth origin data spanned 5 decades and the protocols and practices regarding keeping wild animals in captivity will have changed over time (Kelling and Gaalema, 2011), for example, modern enclosures are often larger and more naturalistic (Maple and Perdue, 2013, Kelling and Gaalema, 2011) and providing environmental enrichment has become more common in recent decades (Mellen and MacPhee, 2001). Since zoos are working to phase out the collection of specimens from the wild (WAZA 2005, IUCN 1993), the wild-bred populations may be older than the captive-bred, thus husbandry practices could be a systematic confound. Consequently the data were analyzed to see if there were systematic differences between the wild- and captive-born populations due to how recently

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Table 1. Species medians by birth origin for locomotor stereotypic behaviour and all stereotypic behaviour

Species SBA N SBA N SBL N SBL N WC CB WC CB

Acinonyx jubatus 35.65 1 18.33 6 35.65 1 18.33 6 Ailuropoda melanoleuca 3.50 2 6.25 5 1.00 1 4.00 1 Caracal caracal 16.37 6 16.37 6 Catopuma temminckii 32.00 1 32.00 1 Felis chaus 12.45 3 12.45 3 Felis margarita 15.00 1 15.00 1 Halichoerus grypus 52.37 10 52.37 10 Helarctos malayanus 25.59 13 26.00 2 Leopardus geoffroyi 24.64 4 24.64 4 Leopardus pardalis 5.18 3 5.18 3 Leopardus wiedii 13.30 1 12.15 1 13.30 1 12.15 1 Leptailurus serval 2.00 2 2.00 2 Lontra canadensis 8.32 1 7.78 1 Lontra longicaudis 20.20 2 20.20 2 Lynx canadensis 6.25 2 6.25 2 Lynx lynx 11.12 9 11.12 9 Melursus ursinus 24.00 1 24.00 1 Nasua nasua 22.74 2 43.48 1 Neophoca cinerea 1.41 1 1.41 1 Odobenus rosmarus 51.27 4 51.27 4 Panthera leo 9.50 9 9.50 9 Panthera onca 8.98 4 19.31 14 8.98 4 19.31 14 Panthera pardus 10.74 7 19.05 8 10.74 7 19.05 8 Panthera tigris 18.41 19 18.41 19 Phoca vitulina 33.24 4 55.21 5 33.24 4 55.21 5 Puma concolor 56.00 1 56.00 1 Puma yagouaroundi 11.84 1 3.00 2 9.08 1 3.00 2 Tremarctos ornatus 36.00 2 36.00 2 Uncia uncia 9.30 6 9.30 6 Ursus americanus 13.00 3 14.52 3 Ursus arctos 80.00 1 19.90 5 80.00 1 19.90 5 Ursus maritimus 35.98 5 26.50 17 35.98 5 26.50 12 Vulpes zerda 5.85 2 5.85 2

Total # species 15 27 15 27

Gaps indicate that no data were available. SBL, locomotor stereotypic behaviour (% obs), SBA, all stereotypic behaviour (% obs.), WC indicates the median for wild-born individuals, CB indicates the median for captive-born individuals. N indicates the number of individuals used to calculate each species median.

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individuals in each populations entered captivity. To do this, the year that a subject entered captivity (either via birth for captive-born individuals or capture for wild-born individuals) was compared between the wild- and captive-born populations.

The number of generations bred in captivity can also be a confounding variable when examining birth/hatch origin effects due to adaptation processes which can occur rapidly (see Chapter 3). It was not possible to determine the number of generations bred in captivity for the majority of the individuals in the stereotypic behaviour database, and excluding the individuals where the generations bred in captivity were unknown would have reduced the already small sample size, thus all individuals were included in the analyses. However it is known that individuals from the semi-domesticated American mink (Neovison vison) and beech martin (Martes foina) have been bred in captivity for their fur for numerous generations and have undergone selection for traits that improve production (e.g. www.furcommission.com/farming/about-mink-farming/). Therefore both of these species were excluded.

Statistical Analysis:

The phylogenetically independent contrasts (see above) were exported into JMP 10.0 for analysis, with all regression lines forced through the origin (see Chapter 2). Analyses were performed to determine whether the slopes of the relationships between the 12 wild behaviour variables and stereotypic behaviour (see Table 1) were significantly different between wild and captive-born populations. This was done by running General Linear Models (GLMs) to test for significant interactions between birth origin and the wild behaviour variables for stereotypic behaviour, controlling for body mass where appropriate. GLMs were also used to compare the severity of locomotor and all stereotypic behaviours between the captive and wild-born populations to determine if there were general effects of birth origin controlling for species. To determine whether the average year animals entered captivity (via birth or capture) differed significantly between the wild and captive-born populations, a GLM was used to test for significant differences according to birth origin for ‘year entered captivity’ while controlling for species. Reported p-values are two-tailed since these analyses were either looking at the interaction with birth origin or there was no specific prediction regarding the direction of the relationship. Appropriate transformations were used when necessary to normalise the data. Statistically significant results were graphed and visually inspected for potential outliers.

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Outliers were confirmed using an online version of the Grubbs test (http://graphpad.com) with alpha set at 0.05 (two-tailed p-value). Confirmed outliers were removed and data were then reanalyzed.

Results

There was no significant difference between the individuals of the captive-born and wild-born populations for ‘year entered captivity’ (F 1,135 =2.29, p=0.1324). Analyses also found no significant differences between the captive-born and wild-born populations in terms of the relationship between each wild behaviour variable to the severity of locomotor stereotypic behaviour and all stereotypic behaviour (Table 2; Figures 1 and 2). Daily distance travelled, home-range size, and chase distance were positively correlated with locomotor stereotypic behaviour in Chapter 2, thus, the models from this chapter that investigated the interaction between birth origin with these wild variable were examined to see if these relationships were still significant within this birth origin dataset. Daily distance travelled (T=-2.30, p=0.0200, d.f. =1,12, one-tailed; significant in opposite direction of prediction) and home-range size (T=1.20, p=0.1215, d.f.=1,20, one-tailed) were no longer significantly correlated with locomotor stereotypic behaviour, and there were insufficient data to look at chase distance. Examining the data for a general effect of birth origin on stereotypic behaviour also found no significant differences between the captive and wild-born populations for locomotor stereotypic behaviour

(F 1,7=0.59, p=0.4674) or all stereotypic behaviours combined (F 1,8=1.65, p=0.2345).

Discussion

Analyses were conducted to test for an interactive effect on stereotypic behaviour between birth origin and aspects of wild behavioural biology in carnivores. Unexpectedly, the captive-born and wild-born populations did not significantly differ in the severity of stereotypic behaviour, and furthermore, no significant differences were found between these sub- populations in terms of their relationships between stereotypic behaviour and the wild behaviour variables. Thus it was impossible to say whether stereotypic behaviour in captive carnivores is

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Table 2. Interaction between the wild behaviour variables and locomotor stereotypic behaviour and all stereotypic behaviours for birth origin

Wild behaviour variables Locomotor stereotypic behaviour All stereotypic behaviours combined

Time spent foraging (% 24 hour) T=0.55, p=0.6105, d.f.=1,4 b T=0.56, p=0.6030, d.f.=1,4 b Trophic level T=-0.55, p=0.5863, d.f.=1,34 a T=-0.44, p=0.6599, d.f.=1,34 a Chase distance (m) insufficient data insufficient data Distance between kills (km) insufficient data insufficient data Hunt frequency (per 24 h) insufficient data insufficient data Kill frequency (per 24 h) T=1.15, p=0.2894, d.f.=1,7 T=1.15, p=0.2894, d.f.=1,7 Diet breadth T=-0.83, p=0.4140, d.f.=1,34 T=-0.97, p=0.3412, d.f.=1,34 Time spent active (% 24 h) T=-0.49, p=0.6281, d.f.=1,17 a T=0.63, p=0.5365, d.f.=1,17 a Home-range size (km2) T=1.20, p=0.2429, d.f.=1,20 a,b T=-0.26, p=0.8002, d.f.=1,22 a Daily distance travelled (km) T=1.35, p=0.2030, d.f.=1,12 b T=1.31, p=0.2138, d.f.=1,12 b Territoriality T=-0.25, p=0.8079, d.f.=1,9 T=-0.26, p=0.8044, d.f.=1,9 IUCN Status T=1.30, p=0.2018, d.f.=1,32 a T=1.63, p=0.1120, d.f.=1,32 a

All p-values are two-tailed a Body mass in model b Outlier removed

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due to CNS dysfunction due to the early environment during development or results from stress, fear, and/ or frustration. Furthermore, since ‘year entered captivity’ (either via birth or via capture) did not significantly differ between the populations, no evidence was found that changing zoo practices over time may have been a confound.

One possible explanation for the lack of results is Type II error: that there were differences between the wild and captive-born populations, but they were not detected in these analyses. Neither home-range size nor daily distance travelled were positively correlated with locomotor stereotypic behaviour in the birth origin dataset, even though these are robust results that were found in Chapter 2 and previous work (Clubb and Mason, 2003, Clubb and Mason, 2007), suggesting the data here were insufficient to detect these results. The sample size was small for many of the statistical models, and furthermore, many of the species medians were also calculated from small sample sizes so they may not be accurate estimates of the true picture (53 of the 84 stereotypic behaviour species medians were calculated with data from fewer than 5 individuals). Furthermore, the data may have also had a lot of ‘noise’ since they were compiled from many sources, and contained individuals with incompletely resolved histories. Thus while attempts were made to control for additional confounds such as rearing history and age entered captivity, this information remained unknown for ~60% of individuals, and due to the already small sample sizes it was not possible to exclude these. This is important because wild-caught individuals that were hand-reared or taken into captivity at a young age would likely resemble captive-born individuals (see Chapter 3); consequently having these individuals included in the analyses would tend to mask any true birth origin effects.

Another possible explanation for the lack of significant results is that there might genuinely be no interaction between natural history and birth origin for stereotypic behaviour: thus birth origin does not mediate or moderate the effects shown in Chapter 2. For example, it could be that motivations to range or to hunt are equally strong in wild-born and captive-born carnivores: not stronger in wild-caught individuals as had been the assumption. Given, however, that there are documented population differences in terms of chronic fear and stress (see earlier discussion above and Chapter 3), as well as cognition and CNS functioning (see earlier discussion above and Chapter 3), this could imply that mechanisms unrelated to stress, fear, or CNS dysfunction underlie the development of stereotypic behaviour in captivity. Alternatively, it could be that these mechanisms are involved in such a way that captive-born individuals and wild-born individuals develop stereotypic behaviour for different underlying reasons (e.g. rearing-induced dysfunction in captive-born versus stress-induced dysfunction in

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80000

60000

40000

Captive Born 20000 Wild Born 0 -20 -10 0 10 20 30 40 -20000

-40000

-60000 Locomotor Stereotypic LocomotorStereotypic Behaviour (%obs) Home-Range Size (km2)

Figure 1. Relationship between locomotor stereotypic behaviour (% obs) and home-range size (km2) controlling for body mass (kg). Each data point represents an independent contrast between two species or ancestral nodes.

5 4 3

2 Captive Born 1 Wild Born 0 -20 -10 0 10 20 30 40 -1 -2 -3 -4 -5

Locomotor Stereotypic LocomotorStereotypic Behaviour (%obs) -6 Daily Distance Travelled (km)

Figure 2. Relationship between locomotor stereotypic behaviour (% obs) and daily distance travelled (km). Each data point represents an independent contrast between two species or ancestral nodes.

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wild-born individuals), but neither group exhibits more stereotypic behaviour than the other. Additionally, many studies that have examined differences in stereotypic behaviour between wild-bred and captive-bred individuals have looked at the prevalence of stereotypic behaviour (the % of population that is stereotypic) (e.g. Jones et al., 2011b, Schoenecker et al., 2000), but not time budget. However the current work in contrast looked at the severity of stereotypic behaviour in stereotypic individuals (% observation time spent in stereotypic behaviour). It is therefore possible that while the prevalence of stereotypic behaviour does differ between the wild-born and captive-born populations (something I could not assess from my data), the severity of stereotypic behaviour exhibited by individuals that do stereotype is similar between the populations.

There are several important avenues for future research that should be explored. Since a number of the high-quality, well-controlled studies discussed previously (see Chapter 3) suggest that being wild-bred may be protective against developing stereotypic behaviour, more research is needed to investigate the relationship between birth/hatch origin and stereotypic behaviour. Increasing both the quantity and quality of data, including more comprehensive data on rearing history and age entered captivity, will be crucial to redoing the current analyses in such a way that they can illustrate the relationship between stereotypic behaviour and birth origin (or lack thereof) with confidence. Additionally, while the mechanisms discussed here specifically relate to stereotypic behaviour, evidence suggests that maturing in captivity, chronic stress, and frustrated motivations may also underlie the development of other abnormalities found in captive animals. Animals housed in impoverished environments may have decreased learning abilities; for example Bell et al. (2009) found an increase in learning abilities and enhanced survival for rats raised in enriched environments as compared to those in standard housing. Stress has also been linked to impaired maternal behaviour (Saltzman and Abbott, 2009, Bahr et al., 1998) as well as impaired immune function (McGlone et al., 1993, Couret et al., 2009). Thus understanding developmental influences on captive animals’ welfare may help give insight into the processes that underlie a wider range of phenomena: it could well be useful to investigate cross-species birth origin effects for other variables, such as infant mortality, reproductive success, measures of health, and mortality rates (see Chapter 3). The infant mortality data used in Chapter 2 could not be used for the birth origin analyses since the birth origin of the dams was not published. ISIS (www.isis.org) was contacted to obtain data that would allow the investigation of these hypotheses for infant mortality; unfortunately this request was declined, so these infant mortality analyses were not possible.

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In summary, no evidence was found to clarify whether stereotypic behaviour in captive carnivores results from forebrain dysfunction due to the early rearing environment or chronic stress, or from fear and frustration. Additionally, no general effects of birth origin were found. It is likely, however, that at least some of these non-significant results reflect Type II errors since the sample sizes were extremely small for many species medians and statistical models. Future research is therefore needed to repeat these analyses with a significantly larger sample size in order to draw sound conclusions about the interaction of birth origin and natural history for captive stereotypic behaviour in carnivores.

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References

Bahr, N. I., Pryce, C. R., Dobeli, M. & Martin, R. D. 1998. Evidence from urinary cortisol that maternal behavior is related to stress in gorillas. Physiology and Behavior, 64, 429-437. Bell, J. A., Livesey, P. J. & Meyer, J. F. 2009. Environmental enrichment influences survival rate and enhances exploration and learning but produces variable responses to the radial maze in old rats. Developmental Psychobiology, 51, 564-578. Campbell, D. L. M., Dallaire, J. A. & Mason, G. J. 2013. Environmentally enriched rearing environments reduce repetitive perseveration in caged mink, but increase spontaneous alternation. Behavioural Brain Research, 239, 177-187. Clubb, R. & Mason, G. 2003. Captivity effects on wide-ranging carnivores. Nature, 425, 473- 474. Clubb, R. & Mason, G. J. 2007. Natural behavioural biology as a risk factor in carnivore welfare: how analysing species differences could help zoos improve enclosures. Applied Animal Behaviour Science, 102, 303-328. Couret, D., Otten, W., Puppe, B., Prunier, A. & Merlot, E. 2009. Behavioural, endocrine and immune responses to repeated social stress in pregnant gilts. Animal, 3, 118-127. Dixon, L. M., Duncan, I. J. H. & Mason, G. 2008. What's in a peck? Using fixed action pattern morphology to identify the motivational basis of abnormal feather-pecking behaviour. Animal Behaviour, 76, 1035-1042. Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist, 125, 1-15. Gittleman, J. L. 1985. Carnivore body size: ecological and taxonomic correlates. Oecologia, 67, 540-554. IUCN. 1993. The World Zoo Conservation Strategy: the Role of the Zoos and Aquaria of the World in Global Conservation. Jones, K. E., Bielby, J., Cardillo, M., Fritz, S. A., O'Dell, J., Orme, D. L., Safi, K., Sechrest, W., Boakes, E. H., Carbone, C., Connolly, C., Cutts, M. J., Foster, J. K., Grenyer, R., Habib, M., Plaster, C. A., Price, S. A., Rigby, E. A., Rist, J., Teacher, A., Bininda-Emonds, O. R. P., Gittleman, J. L., Mace, G. M. & Purvis, A. 2009. PanTHERIA: a species-level database of life history, ecology, and geography of extant and recently extinct mammals. Ecology, 90, 2648. Jones, M. A., Mason, G. & Pillay, N. 2011a. Early environmental enrichment protects captive- born striped mice against the later development of stereotypic behaviour. Applied Animal Behaviour Science, 135, 138-145. Jones, M. A., Mason, G. J. & Pillay, N. 2011b. Correlates of birth origin effects on the development of stereotypic behaviour in striped mice, Rhabdomys. Animal Behaviour, 82, 149-159. Kelling, A. S. & Gaalema, D. E. 2011. Postoccupancy evaluations in zoological settings. Zoo Biology, 30, 597-610. Latham, N. R. & Mason, G. J. 2008. Maternal deprivation and the development of stereotypic behaviour. Applied Animal Behaviour Science, 110, 84-108. Lewis, M. & Kim, S. J. 2009. The pathophysiology of restricted repetitive behavior. Journal of Neurodevelopmental Disorders, 1, 114-132. Lewis, M. H., Gluck, J. P., Beauchamp, A. J., Keresztury, M. F. & Mailman, R. B. 1990. Long- term effects of early social isolation in Macaca mulatta: changes in dopamine receptor function following apomorphine challenge. Brain Research, 513, 67-73. Lewis, M. H., Presti, M. F., Lewis, J. B. & Turner, C. A. 2006. The neurobiology of stereotypy I: environmental complexity. In: Mason, G. & Rushen, J. (eds.) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, 2nd Ediiton. CABI, Wallingford, UK.

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Maddison, W. P. & Madison, D. R. 2006. Mesquite: A modular system for evolutionary analysis. Version 2.75. 2.75 ed. Maple, T. & Perdue, B. 2013. Building ethical arks. Zoo Animal Welfare. Springer, New York, NY. Mason, G. 2006a. Are wild-born animals ‘protected’ from stereotypy when placed in captivity? Box 1, Chapter 7. In: Mason, G. & Rushen, J. (eds.) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, 2nd Ediiton. CABI, Wallingford, UK. Mason, G. 2006b. Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. In: Mason, G. & Rushen, J. (eds.) Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, 2nd Ediiton. CABI, Wallingford, UK. McGlone, J. J., Salak, J. L., Lumpkin, E. A., Nicholson, R. I., Gibson, M. & Norman, R. L. 1993. Shipping stress and social status effects on pig performance, plasma cortisol, natural killer cell activity, and leukocyte numbers. Journal of Animal Science, 71, 888-896. Mellen, J. & MacPhee, M. S. 2001. Philosophy of environmental enrichment: past, present, and future. Zoo Biology, 20, 211-226. Midford, P. E., Garland, T. & Maddison, W. P. 2005. PDAP Package of Mesquite. Version 1.15. Nevison, C. M., Hurst, J. L. & Barnard, C. J. 1999. Why do male ICR(CD-1) mice perform bar- related (stereotypic) behaviour? Behavioural Processes, 47, 95-111. Nyakatura, K. & Bininda-Emonds, O. R. P. 2012. Updating the evolutionary history of Carnivora (Mammalia): a new species-level supertree complete with divergence time estimates. BMC Biology, 10, 31. Presti, M. F., Powell, S. B. & Lewis, M. H. 2002. Dissociation between spontaneously emitted and apomorphine-induced stereotypy in Peromyscus maniculatus bairdii. Physiology and Behavior, 75, 347-353. Saltzman, W. & Abbott, D. H. 2009. Effects of elevated circulating cortisol concentrations on maternal behavior in common marmoset monkeys (Callithrix jacchus). Psychoneuroendocrinology, 34, 1222-1234. Schoenecker, B., Heller, K. E. & Freimanis, T. 2000. Development of stereotypies and polydipsia in wild caught bank voles (Clethrionomys glareolus) and their laboratory-bred offspring. Is polydipsia a symptom of diabetes mellitus? Applied Animal Behaviour Science, 68, 349-357. WAZA. 2005. Building a Future for Wildlife: the World Zoo and Aquarium Conservation Strategy.

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Chapter 5 Final Discussion

This thesis investigated population-level risk factors associated with increased stereotypic behaviour and infant mortality in captive carnivores. Specifically, features of the natural behavioural biology of species were examined as risk factors, while the birth origin of individuals (either captive or wild-born) also was examined as a potential risk factor (in the case of stereotypic behaviour only). Additionally, the data for birth origin were used to investigate the potential underlying mechanisms of stereotypic behaviour in carnivores and a detailed literature review was conducted to examine general birth origin effects across all species. Here, the results are summarized, placed in a broader context, and suggestions given for future research.

Summary of Results

Evidence was found that ranging (home-range size and daily distance travelled) and hunting behaviour (chase distance) in the wild are risk factors for developing stereotypic behaviour in captivity (see Chapter 2). The home-range result replicated previous findings (Clubb and Mason, 2007, Clubb and Mason, 2003), while the chase distance result was new. These two effects appeared to be independent of each other. These results suggest that enrichments related to ranging and hunting behaviour may be important for addressing stereotypic behaviour in captive carnivores. This is useful as stereotypic behaviour is undesirable for a number of reasons: animal welfare (see below and Chapter 1), public education (see below and Chapter 1), reintroductions (see Chapter 1), and also for captive breeding purposes. For example, a recent study has shown that stereotypic male mink are less successful at gaining matings that enriched-housed non-stereotypic animals (Diez-Leon et al., 2013).

In contrast, none of the wild behaviour variables tested predicted increased infant mortality in captivity (see Chapter 2), thus failing to replicate previous work (Clubb and Mason, 2007, Clubb and Mason, 2003). However, whether the original findings of Clubb and Mason (2003, 2007) was a Type I error or that I didn’t find significant relationships was a Type II error, is unknown. This confusion is troubling as infant mortality is very high for many carnivores in zoos (e.g. captive infant mortality rates: lion, Panthera leo, 42%; polar bear, Actos maritimus,

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64%; Pallas’s cat, Felis manual, 91%), so understanding the risk factors would be beneficial. A detailed review of the literature also found evidence that infant mortality tends to be greater for the infants of captive-bred parents than those born to wild-bred parents, and this appears to be partly mediated by poorer parental care by the captive-bred parents (see Chapter 3). Furthermore, the literature review also showed that wild-caught individuals in general seem to be more stressed in captivity than captive-bred conspecifics, while there was some evidence that captive-bred individuals may show some signs of pathology (indicated by malfunctional traits) in terms of brain functioning (see Chapter 3). Both of these results are relevant to understanding stereotypic behaviour (see Chapter 4). When the birth origin data were analyzed to investigate the mechanisms underlying stereotypic behaviour no significant relationships were found, but this may be a Type II error since the available data for analysis were minimal and poor quality (see Chapter 4); thus, it was not possible to gain further information regarding the mechanisms underlying carnivore stereotypic behaviour and its relationship with natural ranging and hunting.

Ranging behaviour and chase distance may be risk factors for the development of stereotypic behaviour, but this does not mean that species which are wide-ranging and hunt prey definitely have poorer welfare in captivity. When multiple measures indicate poor welfare there is strong evidence that there is indeed a welfare concern (as discussed in Chapter 1). Here the wild behaviour variables predicted stereotypic behaviour, but not increased infant mortality; thus it is difficult to draw conclusions regarding welfare. One possibility is that species with small home-ranges and that do not chase prey may simply be expressing poor welfare in a different manner. For example, there is evidence that inactive individuals may be experiencing anxiety or boredom-like states (Meagher et al., 2013) and do not necessarily have better welfare than their more stereotypic conspecifics. This inactivity may be an alternative to stereotypic behaviour (e.g. Mason, 2010). A second possibility is that stereotypic behaviour may stem from brain dysfunction (see Chapter 4), but this may not negatively influence their affective states and thus not impact their welfare (assuming that welfare is about how animals feel: see Chapter 1). It is likely brain dysfunction would impair complex behaviours such as parental care which impact infant mortality (as was suggested for captive-bred animals; see Chapter 3), thus further emphasizing the importance of determining the relationship between infant mortality and the wild variables to help clarify the mechanisms that underlie these results. Understanding the mechanisms that underlie the development of stereotypic behaviour in carnivores, and what the desirable alternate responses to captivity might look like, could help determine if populations

131 with more stereotypic behaviour truly have poorer welfare in captivity. For example, if the underlying causes are primarily related to chronic fear or stress, this may indicate poorer welfare for those individuals, whereas CNS dysfunction would not necessarily impact the affective state of the individual. Another possible mechanism is that certain forms of stereotypic behaviour may be genetically linked to factors such as reproductive output, as was found in deer mice (Peromyscus leucopus) (Lacy et al., 2013), and thus be present as an unintentional side-effect of traits favoured in captivity. Unfortunately, my attempts to investigate these mechanisms were unsuccessful (see Chapter 4). Finally, there is also the possibility that species that do not range widely or chase prey in the wild are adapting well to captivity and have good welfare, and wide-ranging species that chase prey are the ones that should be targeted for management efforts to improve welfare.

Altogether this work shows that certain populations of carnivores may be more susceptible to stereotypic behaviour and possibly decreased welfare in captivity. Wide-ranging and captive-bred individuals show obvious deviations from wild populations in terms of stereotypic behaviour and pathology, and wild-bred individuals have increased stress and fear which indicates poorer welfare. While there is a possibility that wild-born and wide-ranging carnivores thus have poorer welfare due to increased frustrations in their motivations to perform natural behaviours, the data for this were not conclusive. Although zoos are working towards creating self-sustaining populations of wild species and phasing out the collection of specimens from the wild (WAZA 2005, IUCN 1993), the welfare of wild-caught animals may remain a relevant issue for some time: as a result of factors such as expanding human populations and rapid climate change effective conservation efforts may require intensive interventions for wild populations, such as managing them in semi-wild contexts (see below for further details). Clearly, the accumulating evidence illustrates that wild species face numerous issues when held in captivity. Species and populations with known risk factors for issues in captivity should be targeted for increased environmental enrichment, captive welfare studies, and the re-evaluation of captive husbandry practices (these issues are addressed in more detail below). Ethical choices should also be made concerning which species to house in captivity, balancing the welfare of individuals against the needs of species conservation and scientific study. Most importantly, the situations where wild carnivore species are held in captivity should be examined carefully to determine if there is evidence of good welfare and functioning, and sound justifications for keeping those species in captivity.

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Context: a Future for Wild Animals in Captivity?

The practice of maintaining wild animals in captivity as part of the pet trade or for entertainment purposes needs to be examined closely, since these have little justification for education or species conservation. Notably, the inappropriate portrayal of animals appears to cause harm. Ross et al. (2008) found that the portrayal of chimpanzees in the media, such as on TV, was linked to the public’s perception that they were less endangered as compared to other species of great apes. Further studies investigating this effect found that when people viewed pictures of chimpanzees containing images of humans or in typically human settings (such as a business office) or commercials that contained chimpanzees for entertainment purposes, they were more likely to rate the wild population as healthy and stable compared to people who had viewed chimpanzees in species-appropriate contexts (Ross et al., 2011, Schroepfer et al., 2011). Therefore, there is a substantial risk that the public may become complacent about the conservation of a species if that species is viewed frequently in either an inappropriate context or in media without a strong educational message. This suggests that the effectiveness of conservation educational programs and materials in zoos should be carefully evaluated to be sure that viewing endangered species in zoos does not also lead to complacence regarding their conservation needs (see below for further discussion on the educational value of zoos). Similarly, when wild species are housed for research purposes, the benefits of the research should be carefully weighed against the harm to the individual animals. This requires the evaluation of trade-offs between the well-being of individuals versus the potential benefits for a group, whether it be for other members of that species, for humans, for a group of species, or for an ecosystem.

Carnivores are often housed in zoos, as well as in related institutions for ex situ conservation efforts as part of captive breeding and reintroduction programs. Although there are numerous examples where intense ex situ conservation efforts have been necessary and effective (Vargas et al., 2008, Christie, 2009), in many other cases the maintenance of captive individuals or populations have been used primarily for public relations programs even when the conservation value of the captive population is minimal (Hunter et al., 2013). For many species ex situ conservation is not the most effective conservation initiative. Logistical constraints can impede the effectiveness of using captured wild animals for species conservation. There is limited space available to house and support self-sustaining and genetically viable captive populations. In 2005, over 4,000 species of birds and mammals were housed in zoos worldwide (Clubb and Mason, 2007), yet surveys suggest there is only adequate space for 500 species in

133 zoos, with some additional space available in government agencies (Frankham, 2008). As well, ex situ conservation initiatives are very expensive. For example, the annual per capita expense associated with maintaining a captive rhinoceros is approximately ten times greater than the per capita annual cost of in situ conservation (Balmford et al., 1995). Reintroductions with captive- born individuals are generally less successful than the reintroduction of wild individuals (see Chapter 3), and genetic adaptation to the captive environment may occur rapidly (see Chapter 3). A review of reintroduction programs found there were welfare issues associated with 67% of the 199 projects examined, and only ~6% of these studies explicitly addressed animal welfare issues in their studies (although this may be due to underreporting) (Harrington et al., 2013). Thus, there are ethical concerns in the use of reintroductions that involve the release of captive- bred individuals as conservation tools when other alternatives are available and may be more appropriate.

Captive populations may be more useful for educational purposes and fund-raising in support of in situ conservation than they are for actual conservation per se. A survey by the World Association of Zoos and Aquariums (WAZA) found that attendance at zoos globally is greater than 700 million people per year; thus, zoos have a huge potential impact as educational centers (Gusset and Dick, 2011). However, it is not known whether this potential is being translated into effective programs for conservation that actually change visitor behaviours (Ogden and Heimlich, 2009). For example, one study that found a long-term impacts of zoo visitors attitudes towards animals (Falk et al., 2007) but was later criticized for methodological issues (Marino et al., 2010), while some studies have actually found minimal impact (Balmford et al., 2007, Smith et al., 2008). Currently ~$350 million USD are spent world-wide on conservation efforts each year by zoos, and this financial support substantially improves the overall impacts of the conservation initiatives supported (Gusset and Dick, 2010). These impacts would be even greater if other resources, such as expertise on managing small populations, also were given in support of in situ conservation efforts (Gusset and Dick, 2010).

Despite the many advantages of in situ conservation efforts, ongoing issues related to climate change and the current extinction rate will demand that ex situ conservation will play an increasingly important role in species preservation (Pritchard et al., 2012). Some experts are recommending integrated conservation management approaches that combine in situ and ex situ approaches and involve captive, wild, and semi-wild contexts (Minteer and Collins, 2013). More intensive management also will be required in the field with progressive expansion of human development further fragmenting natural habitats, and the expertise gained from captive

134 management will be an important resource in this stewardship (Swaisgood, 2007). Thus, even though in situ conservation initiatives often have a greater impact and are more cost effective, and the primary role of captive collections should be for education and fund-raising, it is likely that the continued housing of some species in captivity for ex situ conservation will remain crucial and valid.

Future Research

It would be valuable to continue to investigate the impact of current educational programs in zoos. As discussed above, some studies have shown that the educational value of zoo animals appears to be either minimal, or is largely untapped, and stereotypic behaviour is thought to reduce the educational value of captive animals (Swaisgood and Shepherdson, 2006). In addition, the frequent portrayal of animals in media (potentially including zoos) might induce complacency and undermine conservation efforts (see above). Future investigations should examine how these programs can be improved, and also whether zoos can have larger scale influences such as influencing career directions and other major lifestyle choices. The results of these investigations would allow for more informed decisions on whether to keep carnivore species in captivity, particularly those at risk of developing issues in captivity, such as stereotypic behaviour or the pathologies outlined in Chapter 3.

A common theme that arose in both Chapter 2 and Chapter 4 is that future investigations into population level risk factors for captive carnivores would benefit greatly from the availability of larger datasets for both stereotypic behaviour and the wild natural history variables (see Chapter 2 for suggestion on how to improve data quality). This would include data for more species as well as more individuals per species to enhance the accuracy of medians as species descriptors. Additionally, it would be beneficial to have a broader representation of taxa within carnivores. Approximately 47% of species in my Captive Carnivore Stereotypic Behaviour Database_2010 were felids, even though felids comprise only 15% of the 286 extant carnivore species (Nyakatura and Bininda-Emonds, 2012). Taxa biases have been reported in zoo research where the distribution of studies across taxa does not reflect the available species, and studies were conducted more frequently on charismatic species (Melfi, 2009). Similar biases have been reported for ecological research as well (Clark and May, 2002, Bonnet et al., 2002,

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Seddon et al., 2005). Felids were also found to be over-represented in the zoo population, where 58% of the individual carnivores housed in captivity are felids although they comprise only 15% of carnivore species (Conde et al., 2011); studies examining snakes, parrots and mammals found that zoo populations were biased towards species rated as being more attractive (Frynta et al., 2010, Frynta et al., 2013, Maresova and Frynta, 2008). These pre- existing biases may explain the abundance of felids in my database since many of these species would be considered charismatic and attractive. Thus, future research should focus on filling in the gaps for underrepresented taxa within the Carnivora to provide a better understanding of the risk factors and behaviour patterns within this taxonomic group.

Future research should aim to tease apart the relative contributions of hunting and ranging: for example, do they predict subtly different forms of stereotypy, or are their effects additive? Furthermore, some alternative motivational explanations for stereotypic pacing remain untested. For example, Clubb and Vickery (2006) suggested that a general need to escape from aversive stimuli may underlie all forms of locomotor stereotypic behaviours. After reviewing the literature they found that observational studies and environmental manipulations tended to provide evidence that either frustrated natural foraging behaviours or a need to escape aversive stimuli led to locomotor stereotypic behaviour, while cross-species analyses supported a link with natural ranging behaviour (Clubb and Vickery, 2006). They concluded that either the biological features underlying each of the different hypotheses may be simultaneously important, or that this general need to escape may underlie all forms of locomotor stereotypic behaviour. This could point towards one mechanism by which hunting and ranging combine to predict pacing: by both elevating motivations to escape. Research investigating the mechanisms underlying the development of stereotypic behaviour, and examining the motivational basis of locomotor stereotypic behaviour, would help clarify these points and provide valuable information for the development of more effective enrichment techniques.

Research also is needed to determine which specific aspects of captivity are linked to the development of stereotypic behaviour and whether these also are correlated with other concerns, such as infant mortality, in captive environments. What aspects of enclosure enrichment are most effective in preventing stereotypic pacing? For example, are there types of enrichment related specifically to hunting and ranging motivations? What aspects of husbandry counteract the development of other forms of stereotypic behaviour in Carnivora; for example, the non-locomotory forms whose risk factors I was unable to identify? Furthermore, should we be looking beyond the characteristics of the main exhibit enclosure characteristics? Positive

136 keeper-animal relationships have been shown to decrease stress (Wielebnowski et al., 2002) and increase reproduction (Mellen, 1991) in felids; a literature review found studies where the size of visitor crowds in zoos increased stereotypic behaviour and decreased activity levels and time spent on exhibit in a wide variety of species (Hosey, 2008); and ambient temperature has been shown to be negatively correlated with stereotypic behaviour in elephants (Rees, 2004) suggesting that climatic variables may also be important. Additionally, the amount of abnormal behaviour exhibited by zoo animals may reflect the fact that they still spend substantial periods of time in relatively barren off-exhibit enclosures; consequently, it would be useful to look at the relationship between stereotypic behaviour and the amount of time spent in barren holding areas or amount of ‘active’ time to control for differences in activity patterns between diurnal and nocturnal species. Off-exhibit holding areas are more comparable to barren lab or farm conditions than the public display zoo exhibits, and this may explain why stereotypic behaviour is still prevalent in zoo populations despite their relatively enriched environments.

To further investigate whether ranging (home-range size and daily distance travelled) and hunting behaviour (chase distance) are reliable predictors of poor captive welfare in addition to stereotypic behaviour, it would be beneficial to closely examine the well-being of species with small home-ranges and species that do not chase prey to determine if they appear to have better welfare in captivity, or are just expressing poor welfare in other ways such as being inactive. If individuals of species with small ranges and species that do not chase prey also have poor welfare in captivity that would predict that the elevated morbidity and mortality may be due to chronic stress. Mueller et al. (2011) elegantly demonstrated how to effectively analyze lifespan with respect to husbandry variables and species-typical risk factors in ungulates, and those methods could easily be adapted to other species such as carnivores (see Chapter 1 for further details). Examination of additional variables such as fertility, and other aspects of reproductive success, would also provide useful information on whether the wild behaviour variables are predictive of broader problems in captivity in addition to stereotypic behaviour.

It would also be valuable to expand the investigations of the relationships between natural behavioural biology and stereotypic behaviour to a more extensive list of taxa. Home- range size has already been suggested as a risk factor for marmosets and tamarins (Mason and Mendl, 1997, Mason, 2010, Prescott and Buchanan-Smith, 2004), while stereotypic behaviour in primates was positively correlated with daily distance travelled, though not home-range size (Pomerantz et al., 2013). Interestingly, this contrasts with the current work in which it was found

137 that home-range size was a more important predictor for stereotypic behaviour than daily travel distance (see Chapter 2). Expanding these types of analyses to other species could also provide useful insights into the mechanisms underlying the development of stereotypic behaviour. For example, the link between the types of stereotypic behaviour and risk factors may prove interesting. In carnivores, the risk factors all involve locomotion (home-range size, daily distance travelled, chase distance) and the most common type of stereotypic behaviour is pacing. It would be constructive to investigate ungulates to see if the major risk factors associated with their predominantly oral stereotypic behaviours (Bergeron et al., 2006) involve foraging behaviours.

Traditionally, animal welfare research has focused on minimizing poor welfare, not on defining good welfare and how to provide it to captive animals (Melfi, 2009, Whitham and Wielebnowski, 2013). There is a growing movement to provide good welfare by promoting positive affective states, and not just the prevention of suffering (Whitham and Wielebnowski, 2013). Arguments have been made that positive life events can off-set aversive experiences (McMillan, 2003, Yeates, 2011) and may be extremely important for overall well-being (Boissy et al., 2007), and thus, useful to identify which species have poor or good welfare in captivity. Many measures of positive welfare have not yet been validated, but suggestions include immune function, heart rate, sleep patterns, and behavioural measures such as play, exploration, affiliative behaviours and vocalizations (Whitham and Wielebnowski, 2013). It would be valuable to use these additional measures to further investigate the relationship between welfare and species typical hunting and ranging behaviour in the wild. This could include investigations of whether species with small home-range sizes, or those that do not hunt, exhibit more signs of positive affective states in captivity. Additionally, it could include the design or fabrication of enrichments that promote positive affective states to help off-set the negative aspects of captivity that are otherwise difficult to alter, for example, enclosure sizes that are substantially smaller than the natural home-range size for wide-ranging species.

In conclusion, population-level risk factors (i.e. birth origin and specific ecological traits) are important for understanding and describing observed differences in how individuals respond to captivity. Notably, there is evidence that wide-ranging carnivores, and those that hunt with long chases, are particularly susceptible to stereotypic behaviour in captivity. Birth origin also potentially predicts some forms of pathology and welfare issues in captivity. My analyses consistently suffered from lack of data, and thus extension of this work with more complete and more comprehensive data would be worthwhile to further investigate natural history and birth

138 origin as population-level risk factors. Future research would provide invaluable information to help assess the ethical implications of keeping wild carnivore species in captivity and also provide information to help understand fundamental biological principles which can be applied to other taxa beyond carnivores.

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