To pace or not to pace? A review of what Abnormal Repetitive Behavior tells us about zoo animal management

Abstract

Performance of Abnormal Repetitive Behavior (ARB) is noted in many captive wild species. ARB can be categorized into two basic forms; those whose aim appears to be to compulsively reach an inappropriate goal, and those whose performance is linked to an inappropriate motor function. While the negative welfare connotations of ARBs are well-known, the precise reason for their performance remains the subject of debate. As zoos move forward in collection planning and to gather more evidence on the biological needs of the species being kept, the idea that ARBs may be part of a “coping function” adds more weight to arguments that some species may not be suitable for the zoo at all. Modern-day definitions of animal welfare tell us to measure the wellbeing of the individual based on its attempts at coping with its immediate environment. A failure to cope, and hence performance of ARB, is an objective and measureable welfare metric that may highlight which species are appropriate for captivity. As conservation pressures on zoos mount, and the need to take in more “captive naïve” species increases, past research on why captive wild animals develop ARB can be used to inform practice. In this paper we aim to review the welfare issues across three basic categories of zoo animal (mammals, birds, ectothermic vertebrates), and critique how research into ARBs can be used by zoos to promote wild-type behavior patterns by providing biologically-relevant management and husbandry regimes, which allow animals the key components of control and choice over what they do and how they do it.

Full text

To pace or not to pace? A review of what Abnormal Repetitive Behavior tells us about zoo
animal management
Paul E. Rose1,2*, Steve M. Nash2 and Lisa M. Riley2
1 Centre for Research in Animal Behavior, Washington Singer Labs, University of Exeter, Perry
Road, Exeter, Devon, EX4 4QG.
2 HE Animal Management, Sparsholt College Hampshire, Sparsholt, Winchester, Hampshire, SO21
2NF
*for correspondence: p.rose@exeter.ac.uk
Running head: captive animal abnormal behaviors
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Abstract
Performance of Abnormal Repetitive Behavior (ARB) is noted in many captive wild species. ARB
can be categorized into two basic forms; those whose aim is to compulsively reach an
inappropriate goal, and those whose performance is linked to an inappropriate motor function.
Whilst the negative welfare connotations of ARBs are well-known, the precise reason for their
performance still remains the subject of debate. As zoos move forward in collection planning and
gather more evidence on the biological needs of the species being kept, the idea that ARBs are
part of a coping function adds more weight to arguments that some species may not be suitable for
the zoo at all. Modern-day definitions of animal welfare tell us to measure the wellbeing of the
individual based on its attempts at coping with its immediate environment. A failure to cope, and
hence performance of ARB, is an objective and measureable welfare metric that may highlight
which species are appropriate for captivity. As conservation pressures on zoos mount, and the
need to take in more “captive naïve” species increases, past research on why captive wild animals
develop ARB can be used to inform practice. In this paper we aim to review the welfare issues
caused by a frustrated motivational needs across three basic categories of zoo animal (mammals,
birds, ectothermic vertebrates), and critique how research into ARBs can be used by zoos to
promote wild-type behavior patterns by providing biologically-relevant management and husbandry
regimes, which allow animals the key components of control and choice over what they do and
how they do it.
Keywords: captive wild animal; zoo animal welfare; Abnormal Repetitive Behavior; evidence-
based husbandry
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Introduction
Abnormal Repetitive Behaviors (ARBs), are observed in many species of captive animal (Garner
and Mason, 2002; Bergeron et al., 2008). Scientists split ARB into two broad categories; those of a
repeated goal-orientated behavior (termed impulsive or compulsive behaviors) and those of a
repeated motor function (termed stereotypic behavior) (Garner, 2008). ARB performance is well
understood, both from experimental work on domestic species and observational studies on
captive wild animals (Broom, 1988; 1991; Broom and Fraser, 2007; Mason, 2010), and they are
defined as behavior whose performance is invariant and inappropriate, and apparently functionless
to the animal (Waters et al., 2002) Some argue, however, that a coping function may be present to
alleviate periods of arousal surrounding stressful events and experience of aversive environments
(Wechsler, 1995; Garner, 2008). As zoos develop away from the “stamp collections” of the past into
conservation centers of the future (Lyles and Wharton, 2013), and as more work on the importance
of exhibit design and best practice husbandry guidelines is performed (Robinson, 1998), the
probability that species will perform an ARB when housed in the zoo should decline. However,
evidence points to situations where the simple fact of being managed affects the species’ ability to
cope and regardless of the quality of its surroundings and care, ARB will still be performed (Mason,
2010; Mason et al., 2013).
Animal welfare as a continuum of emotions and physiologic /psychologic states experienced by the
individual from negative to positive (Boissy et al., 2007; Broom and Fraser, 2007) ultimately affects
biological functioning and fitness (Appleby and Sandøe, 2002). Providing captive animals with a
degree of control over what they do, as well as choice over how they do it (Ross, 2006), is a way of
promoting positive welfare (Hughes and Duncan, 1988b; Yeates and Main, 2008). Species-typical
behavior patterns result from environmental selection pressures (Olsson and Keeling, 2005;
Meehan and Mench, 2007); therefore, husbandry practice and enclosure design will support
positive welfare when considerate of this evolutionary perspective.
Pioneering research from Mason and colleagues tells us that the zoo is not a “common garden”
(Mason, 2010), and that not all species can adapt to the managed environments or husbandry
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regimes provided (Mason et al., 2007). Some species cope better than others when housed in the
zoo. Three qualities are described by Mason (2010) to predict the potential for positive zoo welfare:
i) of being resident in a territory as opposed to highly migratory; ii) being bold rather than shy; iii)
having behavioral plasticity rather than a less adaptable behavior pattern. A deeper understanding
of how and why ARBs develop and are performed enables a better comprehension of how wild
animals control and express their natural/normal behavior patterns (Rushen and Mason, 2008).
Using evidence from natural history and behavioral ecology, such information on “thriving, surviving
or dying” in captivity should be used to inform collection plans and husbandry practice (Melfi,
2009). Pertinent case studies show that environmental complexity (Tan et al., 2013), individuality
(Dallaire et al., 2012), and previous experiences/development (Jones et al., 2011) are all
deterministic factors to the eventual development of ARB in an individual. Examples of such
complexities are provided in individual taxa-specific sections of this article.
As wildlife conservation issues intensity, more species that are novel to the zoo environment may
need direct management in an artificial, ex situ, system. Consequently, an understanding of
naturalistic or normal behaviors is an important way that positive welfare can be underpinned for
the duration of that individual’s / species’ /population’s time in captivity. Research on tigers
(Panthera tigris) that shows ARB performance accounting for nearly a quarter of an individual’s
time budget (Mohapatra et al., 2014) clearly demonstrates the need to resolve husbandry factors
for commonly kept species, even in the 21st Century, on top of researching how “new to the zoo”
species should be managed.
In this review we aim to explore how research on ARBs can be turned into action to help those in
zoos understand the needs of their animals and ultimately consider behavioral ecology. We
suggest ways of informing collection plans and future husbandry provision for the myriad of
species that zoos may be called upon to look after, and we aim to evaluate ways of reducing /
eliminating species-specific ARBs where they still occur. While we cannot cover all species housed
in the modern zoo, we attempt to evaluate pertinent research into mammals, birds, and
ectothermic vertebrates (reptiles, amphibians and fish).
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Abnormal behavior in zoo-housed mammals
Primates: Apes and Old World Monkeys
Research on ARBs has focused principally upon mammals and in a zoo setting primates,
carnivores, elephants, and, to a lesser extent, ungulates have been studied. These taxa will be the
focus of discussion here. Quantitative studies remain rare (Pereboom and Stevens, 2015),
however ARBs are often part of rearing and enrichment studies where primates receive much
attention (Buchanan-Smith, 2010). Behavioral pathology in apes and Old World monkeys is
relatively well understood, especially in chimpanzees (Pan troglodytes) (Brüne et al., 2004; Brüne
et al., 2006). Birkett and Newton-Fisher (2010) compiled a list of 37 abnormal behaviors in captive
chimpanzees from literature and direct observation, ten of which were defined as repetitive or
stereotypical (e.g., “rock”, “self-groom stereotypically”, “self-groom with object”, “rub hands”,
“pace”). Sixteen additional behaviors, such as “pluck hair, “bounce”, “twirl” and “head toss”,
logically involve repetitive actions. Forty group-living individuals housed in six industry-accredited
zoos were studied and all performed ARBs, on average 18 different types per group, with the
behaviors “rock”, “groom stereotypically” and “pat genitals” being the most prevalent. Given that
this research was conducted on both laboratory and zoo populations, findings suggest that the
enhanced provisions in many zoos do not fully safeguard against the development of stereotypies
that are common in more barren environments.
Whilst some dietary generalist species typically adapt well to captivity, this is not a wide-ranging
statement across the primate order (Mason et al., 2013). Other great apes demonstrate ARB in
captivity which, as in chimpanzees, are often associated with self-injurious behavior (Lutz et al.,
2003). Bonobos (Pan paniscus) have shown a 93% prevalence of abnormal behavior (Pereboom
and Stevens, 2015), particularly hair plucking stereotypy (Brand and Marchant, 2015).
Regurgitation and reingestion in western lowland gorillas (Gorilla gorilla gorilla) is well documented
(Lukas, 1999; Hill, 2009), but Blaney and Wells (2004) also report stereotypic teeth clenching,
rocking, and spinning in zoo-housed gorillas, providing other behavioral avenues of welfare
investigation.
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ARB performance in Old World monkeys is also widely noted. A longitudinal laboratory-based
study of over 3,800 captive rhesus macaques, Macaca mulatta (Gottlieb et al., 2015) found
stereotyped motor patterns to be widespread. Lutz et al. (2011) additionally reported bouncing,
somersaulting, rocking and swaying in this species and hence it is clear that ARBs in primates are
diverse and prevalent. Table 1 outlines the risk factors associated with the development of ARBs,
alongside of remedial husbandry tools for these taxa.
TABLE 1 GOES HERE
Table 1. Summary of major risk factors and potential solutions to the development of stereotypic
behavior and ARBs in apes and Old World monkeys.
In a comprehensive review of the socio-ecological correlates of stereotypic behavior in 24 species
of zoo-housed primates (Pomerantz et al., 2013) natural group size is identified as a risk factor for
development of stereotypic hair-pulling. Stereotypic pacing was significantly positively correlated
with natural daily journey length. Thus species which in the wild travel further per day and live in
larger groups may be more likely to have compromised welfare in captivity unless these intrinsic
needs can be met. The authors advocate provision of appropriate social stimuli and complex
physical environments, and consider the onset of ARB may be explained by a lack of ability to
explore and problem solve in a suitably complex environment. Such findings are similar to those
from carnivore welfare research based on natural biological risk factors for ARB (Clubb and Mason,
2003; 2007).
An individual can become so reliant on behavioral psychopathology that it gives no response to
careful re-socialization or environmental enrichment when this is provided (Swaisgood and
Shepherdson, 2005; Brüne et al., 2006; Rommeck et al., 2009. ARBs may develop as a latent
response to maternal deprivation and inadequate early rearing environment (Ellenbroek and Cools,
2002; Latham and Mason, 2008. A growing body of evidence suggests zoos should rear primates,
particularly great apes, with their mother (and father, as appropriate) past the age of behavioral
independence, in a stimulating and complex physical and social environment that affords
individuals choice, control and learning opportunity – which mimics their natural rearing situation -
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as this can safeguard against ARBs (Latham and Mason, 2008; Newberry and Swanson, 2008;
Prescott et al., 2012; French and Carp, 2016).
Carnivores: bears and big cats
Like primates, ARBs of carnivores are well documented. Motor stereotypies (e.g. weaving, pacing)
have been observed in captive polar bears, Ursus maritimus (Clubb and Mason, 2003;
Shepherdson et al., 2013; Cless et al., 2015), lions, Panthera leo (Clubb and Mason, 2003), brown
bears U. arctos (Montaudouin and Le Pape, 2005), spectacled bears, Tremarctos ornatus (Maslak
et al., 2013), clouded leopards, Neofelis nebulosa (Wielebnowski et al., 2002), snow leopards, P.
uncia (Macri and Patterson-Kane, 2011), tigers (Miller et al., 2008), and ocelots, Leopardus
pardalis (Weller and Bennett, 2001).
Clubb and Mason (2003) found that bears display the highest frequency (proportion of observed
time) and prevalence (percentage of individuals affected) of stereotypic behavior compared to
canids and felids. Zoo-housed polar bears spend 11-30% of their time pacing (Clubb and Mason,
2003; Shepherdson et al., 2013). Mean polar bear home range size can be 125 100 km2 (Ferguson
et al., 1999) and captive bears can experience a living area one millionth of the size of what they
would inhabit in the wild (Clubb and Mason, 2003). Polar bear stride length is significantly shorter,
head height significantly higher and gait variation significantly reduced in stereotypic pacing
compared to normal locomotion (Cless et al., 2015). An extreme example involving spectacled
bears housed in a severely size-restricted and very basic enclosure in a European zoo documents
one animal spending a median 57 min/hour performing ARB (Maslak et al., 2013). The two bears
studied performed less stereotypy when moved to a complex, larger exhibit, and when provided
with dental treatment. Though a wider sampling period was required, this research highlights the
need to improve carnivore husbandry guidelines. The need to develop management and
husbandry strategies (inclusive of enclosure design and environmental enrichment planning) that
equally integrate physical and psychological health care is paramount. Guidelines could,
progressively, substantiate minimum space requirement with optimal enclosure complexity
(quantity and quality of space) recommendations.
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Seminal research has identified larger, more wide-ranging carnivore species spent increased time
performing ARBs compared to smaller carnivores with more restrictive ranges (Clubb and Mason,
2003; 2007). Larger body sizes and longer daily travel distances were also identified as risk factors
for ARB performance across carnivores (Clubb and Mason, 2003; 2007). Such research helps
zoos to review the reasons for keeping large carnivores in captivity on ethical and welfare grounds,
as well as to decide how to best keep species based on scientific data. Inevitably there will be a
conservation need to maintain polar bears and alike in captivity, and hence research needs to be
directed towards dramatically improving welfare. Like for primates, research suggests the need for
large, complex enclosures to uphold excellent bear welfare, e.g. use of tools and complex
enrichment for brown bears (Waroff et al., 2017). Interestingly, Waroff et al. (2017) found that
source of bear and history affected the extent to which they used complex equipment, and
therefore the affect the potential beneficial effects of such enrichment. ARB performance in polar
bears is negatively correlated with enrichment, number of animals in the exhibit, and whether the
bears can see out of their enclosure (Shepherdson et al., 2013). Fecal glucocorticoid concentration
is positively correlated with pacing and negatively correlated with dry-land exhibit area. These
authors advocate increased provision of dry-land areas, increased use of environmental
enrichment, and visual access out of the enclosure to promote physical and mental health of
captive polar bears.
Brown bears that paced, circled or head-tossed, and who are older animals housed indoors
overnight with a restrictive feeding pattern, appear more likely to express ARB (Montaudouin and
Le Pape, 2005). In addition, the amount of ARB was significantly lower when bears have access to
a pool, but group size has no effect on ARB performance. As such, the requirements for species-
appropriate husbandry and enclosures is rationalized. Based on the evidence evaluated here, zoos
should provide pools, large dry-land areas, long-range visual access, diverse environmental
enrichment, 24-hour access to outdoor enclosures (Ross, 2006), and multiple daily feeds.
ARB risk factors for clouded leopards include a lack of exhibit height and hiding spaces
(Butterworth et al., 2011), while in cheetah (Acinonyx jubatus) and tigers small enclosure size,
solitary living, predictable feeding regimes, visual access to others, and (specifically for tigers) lack
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of access to a pool increased prevalence of ARBs (Miller et al., 2008; Quirke et al., 2012; Breton
and Barrot, 2014; Biolatti et al., 2016). As such, to improve zoo-housed carnivore welfare, more
space, multiple dens, and greater day-to-day environmental complexity should be provided
(Mason, 2010). New research also suggests that some individual captive tigers can be as active as
wild conspecifics, and that an individual’s need for movement may be an essential consideration in
some large felids (Breton and Barrot, 2014). Greater consideration for measurement of species-
specific and individual welfare in big cats is needed due to large variation in body size and ecology
(Whitham and Wielebnowski, 2013) that may make general welfare metrics less relevant to all
taxa. Complex climbing opportunity, increased privacy and hiding opportunity, multiple daily feeds,
no visual access to others and species-specific social environments may help to enhance the
positive experiences for captive big cats.
Elephants
Both Asian (Elephas maximus) and African (Loxodonta africana) elephants are prone to
development of ARBs in captivity (Wilson et al., 2004; Mason and Veasey, 2010). ARB
performance appears to have a direct, negative effect on individual elephant health too. A survey of
captive Asian elephants found 59 of 87 elephants to have foot problems (e.g., arthritis, split nails,
abscesses), 53 of which displayed ARBs (Haspeslagh et al., 2013). Prevalent ARBs included
weaving (most prevalent at 37% of elephants), swaying, nodding, head bobbing, trunk swinging,
foot lifting and pacing. Frequency of pacing, head swaying and weaving can be higher in the
afternoon and on colder days, and when animals were anticipating feeding (Rees, 2004).
Advancing age also affects predisposition to ARB performance (Haspeslagh et al., 2013). Such
evidence demonstrates the complex multifactorial influences, of the individual and the
environment, on the development and performance of ARB in these two species.
Maternal deprivation, which has a profound effect on primate welfare has largely been ignored in
relation to ARB development in elephants. Like primates, elephants have extended life histories. In
captivity elephant calves can be separated from their mothers when nutritionally weaned around
three years old (Clubb and Mason, 2002), whereas wild male calves may remain with their mothers
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until 10–15 years old (Eisenberg et al., 1971) and females remain for life (Sukumar, 1989). This
may be a risk factor in the development of ARB in zoo elephants and warrants further research. As
both elephant species face acute conservation threats it is pertinent to conserve not just genetic,
but behavioral diversity, including their wild-type behavioral repertoire (Cameron and Ryan, 2016).
The learning opportunity afforded by mothers may buffer against development of ARBs, as it does
in primates (Latham and Mason, 2008).
Ruminants
Anecdotally, evidence for oral and motor ARBs in captive ruminants is prevalent yet they remain
poorly empirically studied. In a survey of captive giraffe (Giraffa camelopardalis) (N=214) and okapi
(Okapia johnstoni) (N=29), Bashaw et al. (2001) found nearly 80% of giraffe performed ARBs,
specifically licking non-food object and pacing. Subspecies, number of hours spent indoors, access
at night to conspecifics, and feeding frequency, method of feeding and type of food provided were
predictors of stereotypic licking, whereas subspecies, birth history, size of the indoor enclosure,
environmental change, and type of food provided were found to be significant predictors of
stereotypic pacing. Like elephants, the complexity of ARB development in these two species is
complex.
Case studies on two giraffes showed that increased dietary fiber significantly reduced time spent
performing oral stereotypes and increased time spent ruminating. Hence, to improve giraffe
welfare, zoos should provide rumination opportunity by increasing dietary fiber (Baxter and
Plowman, 2001) and provide environmental enrichment that promotes complex, natural tongue-use
(Fernandez et al., 2008). However, in the giraffe, specifically, care should be taken to not overly
restrict concentrate pellet intake, which may lead to nutritionally-related pathology and an inability
to meet energy demand (Clauss et al., 2006; Rose et al., 2006). Zoos should also systematically
research oral and motor stereotypy in ruminants to further identify targeted and evidence-based
approaches to alleviating ARBs. To this end, collaboration with educational establishments
(Fernandez and Timberlake, 2008) can help zoos set-up and maintain both short- and long-term
research projects. Such efforts can help meet legal research and welfare responsibilities, for
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example those detailed in the Secretary of State’s Standards for Modern Zoo Practice in the United
Kingdom (Department for Environment, Food and Rural Affairs, 2012).
Across mammals it is clear that enhanced environmental enrichment is needed to encourage
diverse, natural behavioral repertoires (Maple, 2015). There are opportunities for zoos to improve
(Mason 2010) using a framework provided by Mason et al. (2007). Only 50% of environmental
enrichment attempts may succeed in reducing ARBs (Swaisgood and Shepherdson, 2005). To
reduce the prevalence and frequency of ARBs in mammals, zoos must develop species-specific,
individualized, solution-specific enrichment programs (Mellen and Sevenich MacPhee, 2001; Melfi,
2009), not simply generic schedules of enrichment. Zoos must maintain the maternal-infant bond
and support social or familial stability across generations, providing enriched rearing opportunities
and the opportunity for captive-born individuals to educate themselves in how to raise their own
young in the future. Zoos may face an ethical dilemma of not breeding from hand-reared
individuals or those exhibiting ARBs. Hand-reared parrots are more likely to suffer from ARB and
have impoverished welfare when housed in captivity, and are more averse to interacting with
enrichment (Williams et al., 2017). Similar patterns for mammals may be elucidated.
Abnormal behavior in zoo-housed birds
ARBs in caged birds are well documented (Fox, 1968; Keiper, 1969; Greenwell and Montrose,
2017), but there is comparatively little research on their causal factors and long-term effects (van
Hoek and Ten Cate, 1998). Repetitive perch hopping or route-tracing in caged passerines (Keiper,
1970) after a stressful event indicates that behavioral disturbance can be linked to acute stress.
The authors have observed head rolling in Gouldian finches (Erythrura gouldiae) in the same
circumstances. The latent effect of a stress response and the time taken for ARB performance to
decline and cease may be a reliable indicators of coping in captive birds.
Negative affective states (NAS) as indicators of stress and suffering (Meehan and Mench, 2007),
widely described in mammalian species, are noted in birds and have direct effects on
psychological and related physical health of captive individuals. Research on pessimistic traits in
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aviary-housed starlings (Sturnus vulgaris) shows both both individual and environmental (provision
of enrichment) effects on ARBs (Brilot et al., 2010), demonstrating that personality and mood of
captive birds can be negatively altered by barren or unstimulating enclosures. As with captive
mammals, captive birds can have their welfare improved via the use of appropriate environmental
enrichment (King, 1993; Young, 2003). Aviary furnishing and perching styles are important
components for avian welfare (Rose and Cameron, 2012). Flighted birds, or those that like to climb
can have their quality of life improved by use of appropriate perching styles that mimic the
important natural features. Quality space- which includes furnishings and resources within the
enclosure, rather than just size (Hediger, 1950) - is an important consideration for both flighted and
flight-restrained species, as has been recognized for commercially reared chickens. Birds that are
kept flight restrained can still behave in a naturalistic fashion if consideration is given to provision of
a varied habitat for behavior to be performed (Rose et al., 2014a).
As an example of NAS manifesting as performance of stereotypies, obvious and well-known ARBs
occur in parrots (Psittaciformes) (Garner et al., 2003b; Greenwell and Montrose, 2017). Highly
injurious and debilitating conditions can develop, including screaming and repetitive vocalization,
self-mutilation, bird-directed and human-directed aggression, neophobia, phobias of people, places
and environments, inappropriately-directed sexual behavior, and feather damaging behaviors
(Garner et al., 2003b; van Zeeland et al., 2009). If parrots and other birds can experience NAS,
work on maintaining positive affective states (PAS) should be a priority. Welfare metrics in captive
species can be difficult to determine, as many traditional methods lean heavily on human-focused
modalities (Mason and Veasey, 2010). PAS in bird may rely on better understanding the need for
the performance of behaviors linked to deeper psychological welfare.
The concept of ARB development due to “frustration” from an inability to perform a goal-orientated
behavior (Hughes and Duncan, 1988b) is as apparent in birds as in mammals (Jensen and Toates,
1993; Vinke et al., 2008). Seminal research on domestic fowl (Gallus gallus domesticus) shows
that stereotypic behavior and sham nest-building occurs when nest building behavior is thwarted
(Hughes and Duncan, 1988a). Environmental conditions can reduce an individual’s ability to
perform specific goal-orientated behaviors (Polverino et al., 2015), resulting stereotypic actions are
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the result of unnatural selection pressures on birds in captivity (Hawkins, 2010). Birds must be
provided with appropriate outlets for their entire range of species typical behaviors in captivity, and
use of enrichments and functional replication of habitat features is one way this can be achieved.
The comparative approach of assessing species responses to captivity (Mason, 2010; 2015) that
underpin husbandry and housing decisions by using empirical evidence (Melfi, 2009) helps
manage species by being sympathetic to their ecology and evolutionary biology. Comparison of
behaviors of captive ducks in order to determine species-specific time budgets inside and outside
of the molt revealed that zoo-housed birds alter activity in the same way as free-living birds
(Portugal et al., 2010). The physiological responses to molt were not affected by being captive.
Using data on wild behavioral rhythms as a baseline for assessing individual species is a simple
way that positive welfare of captive birds can be measured. Calculating activity patterns of
representative species of duck and goose shows there to be very little difference in time allocation
to state behaviors when compared to free-living individuals (Roper, 2015). Utilizing such data on
activity patterns can permit birds managed in captivity to be given the same options that wild birds
have to regulate behavior patterns.
Similar behavioral problems can be seen across different avian taxa. Feather damaging behaviors
(FDBs) in birds can include feather pecking, as described by the redirected ground pecking
hypothesis (Blokhuis, 1986) in poultry. Feather plucking or pterotillomania in parrots (Lumeij and
Hommers, 2008) has similar outcomes for affected individuals. Predictability has been associated
with development of ARB in domestic fowl (Savory and Kostal, 1996). Different forms of abnormal
behavior are noted before and after the predictable event has occurred. The timing of events in the
day or across the year can be manipulated to encourage the performance of naturalistic behavioral
rhythms in many avian species in captivity.
Many species of bird undertake predictable seasonal migration, and such highly synchronized
movement is under the control of exogenous (e.g., light and temperature) and endogenous (e.g.,
endocrine) factors. Research on behavioral and physiological change associated with the onset of
the migration period has shown elevated activity in greenfinches (Chloris chloris) and snow
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buntings (Plectrophenax nivalis) (Krüll, 1976). Such work may be helpful to those managing
migratory species in the zoo and interventions to manage behavior made to alleviate any stress or
potential for negative welfare state. Birds use environmental conditions to initiate specific behaviors
(Shariati-Najafabadi et al., 2016), so the effect of an artificial or controlled environmental variables,
such as lighting, on important behaviors should be considered (Avey et al., 2011). Research into
the effect of fluorescent lighting flicker speed on starling behavior shows that mate choice
decisions can be compromised (Evans et al., 2006), that birds will show behavioral and
physiological signs of chronic stress (Evans et al., 2012), and that welfare is adversely affected
upon by use of artificial lighting designed for human eyes (Greenwood et al., 2004). Factors other
than aviary size, furnishings, and inhabitants influence whether a species is predisposed to
performance of ARB, and such factors (e.g., types of lighting used, and how a season is artificially
manipulated) should be evaluated for promoting positive welfare states and reducing ARBs in
captive wild birds.
Route pacing in caged blue tits (Parus caeruleus) and marsh tits (P. palustris) results in the
wearing of feathers due to repeated contact between the feather and the bird’s cage (Garner et al.,
2003a), demonstrating how observable changes to body condition can result from ARB
performance. Season will still affect motivation to travel in migratory species, despite caging
(Dawkins, 2004). Past research counting footprints on blotting paper showed that captive warblers
will move more in the build-up to times when they should be travelling to new climates (Birkhead,
2012). Given the large number of migratory birds held in zoos, positive welfare states could be
benchmarked if research established species most prone to disturbed time budgets related to the
migration period.
Social networks and social support are important concepts of positive welfare for many captive
species (Makagon et al., 2012). Numerous species of birds occur in large flocks, so the
maintenance of long-term bonds and individual partner preference can improve individual welfare
state and promote natural behavior patterns (Seibert, 2006; Rose and Croft, 2015). Disruption to
social structure, including that imposed by inappropriate housing, manifests as ARB in psittacine
species (Polverino et al., 2012; Polverino et al., 2015). In budgerigars (Melopsittaccus undulatus)
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solitary-housed birds are more likely to be neophobic (Nicol and Pope, 1993), an effect of altered
exposure on behavioral development in a highly social species. Increased aggression and reduced
reproductive output is seen in great Indian hornbills (Buceros bicornis) associated with mate
incompatibility adversely affects breeding programs (Kozlowski et al., 2015). Amazon parrots
display limited behavioral complexity and reduced reproductive output when housed in a social
environment over which they have no control over (Meehan et al., 2004). Lower corticosterone in
breeding compared to non-breeding hornbill pairs (Crofoot et al., 2003) demonstrates the
importance of a settled, stress-free environment to the successful reproduction of such sensitive
species in captivity. Aggression between a male and female hornbill in a pair indicates
incompatibility (Saad and Rasip, 1995). Heightened levels of conflict divert energy away from
essential parts of courtship display, and can be deemed abnormal behavior as such aggression is
not conducive to the animal’s desire to breed, Great Indian hornbills are “Near Threatened”
(BirdLife International, 2013) and so are an important focus for avian conservation in zoos (Collar
and Butchart, 2014). If husbandry methods negatively affect productive output, the goal of a
sustainable zoo population and ex situ conservation is thwarted.
For positive avian welfare to be promoted and maintained, zoos should work to recreate functional
habitat that aids in formation of appropriate flock structure and occupational enrichment (Figure 1).
Such changes should diminish ARB.
FIGURE 1 GOES HERE
Figure 1: promoting positive welfare in captive wildfowl by maintaining birds in appropriate social
groups and by replicating key habitat features linked to important aspects of behavioral ecology. In
this case, common goldeneye (Buchephala clangula) kept on clean water deep enough to allow
diving and underwater swimming, and in a mixed sex flock that facilitates performance of courtship
display.
Abnormal behaviors in zoo-housed reptiles, amphibians and fish
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The current conservation status and associated need for increased in-zoo management of many
non-mammalian or non-avian vertebrate taxa adds an urgency to the development of husbandry
protocols based on sound empirical evidence (Michaels et al., 2014b). Behavioral diversity should
be considered with genetic and species diversity when setting conservation priorities (Angeloni et
al., 2010). Reptiles, amphibians and fish are under-represented in research on behavioral diversity
and needs (Hosey et al., 2009). This lack of data pertaining to captive welfare (Greenburg, 1995)
contributes to the historic lack of enriching environments in zoos (Burghardt, 2013). The
phylogenetic distance of these taxa from humans may reduce intuition about behavioral
abnormalities and the appropriateness of the containment environment (Rosier and Langkilde,
2011).
The innate nature of ectothermic vertebrate behavior requires specific environmental conditions.
Basic ecological and ethological knowledge for many commonly kept species is restricted
(Arbuckle, 2013) and contributes to a lack of information on wild and captive time budgets
(Burghardt, 2013). These taxa are species rich, implying considerable inter- and intra-specific
variation. Behavioral divergence of captive animals from their wild counterparts has been
documented (McPhee, 2004; Kelley et al., 2006), and appears to manifest itself as an absence of a
normal behavior in ectothermic vertebrate, rather than in ARBs (Michaels et al., 2014a). Little
evidence exists to document ARBs in fish and amphibians, as enrichment needs are typically met
by the provision of more naturalistic environments within specified environmental parameters. In
addition, we may not understand the behavior patterns of these species in sufficient details to note
and identify ARBS when they occur out of context.
Surface breaking behavior in captive rays (Raja sp.) is one of the most widely reported fish
aberrant behaviors. Scott et al. (1998a) suggests that this behavior may be linked to hunger and
represent et-epimeletic behavior; however, the behavior is reduced by providing food in a manner
that allows benthic feeding, the species-typical behavior (Scott et al., 1998b). Behavioral and
activity patterns are complex, and species typical needs and behaviors must be understood within
these contexts.
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Captive reptiles have gained a reputation as “stoic automatons”, unremitting stimulus-response
creatures with a tendency towards behavioral inertia (Burghardt, 2013). This is in stark contrast to
wild individuals that can demonstrate a behavioral diversity akin to that of mammals and birds
(Wilkinson et al., 2010a; Wilkinson et al., 2010b; Wilkinson and Huber, 2012). The ectothermic
metabolism of these animals dictates that all activity is determined by the thermal parameters that
link physiology, ecology and behavior (Huey, 1991). Thermal heterogeneity allows behavioral
optimization of physiological processes that are temperature dependent (Wilms et al., 2011), and
inappropriate thermal environments constrain the expression of non-maintenance behaviors as the
animal struggles to meet its core metabolic needs.
A captive environment that fails to provide the thermal and structural complexity required by a
given species will be unable to provide the conditions necessary for a full, natural behavioral
repertoire to be displayed. Rose et al. (2014b) demonstrate the importance of both structural and
thermal heterogeneity for captive corn snakes (Pantherophis guttatus) and chuckwallas
(Sauromalus ater). The provision of choice enables animals to utilize their environment in a way
that befits their needs. Health issues such as thermal burns and rostral abrasions are prevalent in
captivity, but non-existent in nature, and indicate the lack of understanding of specific requirements
of such taxa. Welfare issues may arise from “controlled deprivation” (Burghardt, 2013), i.e.,
reduced environmental complexity and stimuli in captive environments when compared with
nature. It is the role of the keeper to identify and provide the most salient features possible, based
on restricted evidence. The tendency to maintain captive reptiles and amphibians under
comparatively simple, size-restricted conditions, particularly for animals housed off-exhibit in zoos
may be based on inappropriate “evidence”. For example, sedentary behavior is typically transient
following the consumption of a meal, and should not be used as the sole basis for determining
spatial needs (Warwick et al., 2013). The largest herptile specimens are most often housed in the
smallest enclosures relative to their size. Large Boidae snakes are often maintained in captive
conditions that do not permit straight line posture (Nash, 2016b). Such an approach minimizes the
snake’s opportunities to display a wide range of behaviors and exacerbates health issues due to
enforced immobility (Scott, 2016). A lack of peer-reviewed literature on this issue highlights the
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need for further research on husbandry so that normal behavior patterns are displayed by these
species when housed in captivity (Arbuckle, 2013; Nash, 2016a).
Seemingly complex, enriched environments may be provided for aesthetic viewing display, while
not truly meeting the animal’s needs (Burghardt, 2013). Sterile housing conditions are likely to
result in elevated stress levels for the inhabitant (Mendyk, 2015). Typical indictors of stress include
behavioral inhibition and reduced behavioral complexity, heightened vigilance, hiding, aggression,
decreased exploratory behavior, and hyper- and/or hypo-activity (Morgan and Tromborg, 2007;
Warwick et al., 2013). That use of behavioral husbandry can reduce stress and negative behavior
is demonstrated in Xenopus frogs where aggressive behavior and cannibalism is reduced by the
provision of refugia (Torreilles and Green, 2007).
Perimeter pacing and interactions with transparent boundaries (ITB) are frequently seen in many
taxa and both can be explained by inadequacies in the captive conditions. Ethologically-informed
vivarium design is important in eliminating ITB in chuckwallas (Rose et al., 2014b). Perimeter
pacing and ITB are widely reported in Varanidae. Daily movements of over 180m are reported in
small Varanus species in the wild, and home ranges can be 40.3 Ha (Thompson et al., 1999).
Home range variation in Varanidae can also be dependent on habitat type and sex (Smith and
Griffiths, 2009), and ontogeny (Imansyah et al., 2008). Perhaps there is a parallel for these highly-
mobile, behaviorally flexible lizards (Gaalema, 2011) in Clubb and Mason (2003)’s seminal work on
mammalian carnivore stereotypy and range size? Carfagno and Weatherhead (2008) recorded
variation in daily distances travelled in snake species and found that eastern racers, Coluber
constrictor, travel 88 m/day compared to 23.1m/day for the black rat snake, Elaphe obsoleta). Such
travelling distances are greater than typical vivarium dimensions allow, but are insignificant when
compared to the migratory patterns of loggerhead sea turtles (Caretta caretta) and other pelagic,
diving species (Polovina et al., 2004).
The importance of environmental complexity varies across taxa. Zebra danios (Danio rerio) and
checker barbs (Puntius oligolepis) show clear preferences for enriched environments (Kistler et al.,
2011), but determination of behavioral diversity in these two species may be more complex. Wilkes
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et al. (2012) suggest that enhanced environments do not result in measurable welfare
improvements for zebra danios, highlighting the individuality of species’ needs in captivity as well
as the need for appropriate measures for determining good welfare in said species. Results of
enrichment research for lower vertebrates is highly dependent on the type of enrichment or
environmental complexity provided to the animal (individual and species) being tested, and thus
parallels that conducted on “higher vertebrates”.
Animals in complex and enriched environments show enhanced foraging efficiency and exploratory
behavior (Almli and Burghardt, 2006). A preference for complex environments in eastern box turtles
(Terrapene carolina) presents as a reduction in escape behaviors combined with positive
physiological differences (measured as a reduced heterophil to lymphocyte ratio) when compared
to counterparts in barren environments (Case et al., 2005). Research on clawed frogs (Torreilles
and Green, 2007) demonstrates that comparatively simple husbandry modifications such as the
provision of multiple refugia, can positively affect behavior (in this instance by reducing the
incidence of agonistic behaviors between conspecifics). However, such ‘simple’ modifications may
not be as simple as they first appear. Refuge selection in free-living terrestrial taxa relies on
assessment of temporally variable parameters such as thermal and hydric properties, and
structural features such as size (Webb et al., 2004; Croak et al., 2008). Overall, such research
indicates that refugia in a captive setting promotes the opportunity for choice, with its associated
welfare benefits.
Elevated stocking densities and spatial restriction have been implicated as causal factors for
elevated stress levels and aggression towards conspecifics (Ashley, 2007), yet these behaviors are
also observed in shoaling fish species kept at low densities (Saxby et al., 2010). Overcrowding
results in overt and covert responses (Warwick et al., 2013) with the former relating to the physical
number of animals in a given space and the latter to the ability of all animals to access all features
of the space. Captive-bred butterfly splitfins (Ameca splendens) display higher levels of aggressive
behavior than their wild born counterparts in response to these factors (Kelley et al., 2006).
Territoriality, exploratory behavior and social behavior may also be impeded (Angeloni et al., 2010)
under such overt conditions. Shoaling behavior may provide opportunities for social learning, as
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demonstrated in guppies (Poecilia reticulata) (Laland and Williams, 1997; Swaney et al., 2001;
Croft et al., 2006), and so provide opportunities for enhanced behavioral repertoires. New research
shows the existence of a complex social system in veiled chameleons (Chamaeleo calyptratus),
with sociality being shaped by early life interactions (Ballen et al., 2014). If, as seems likely, social
rearing affects the development of subsequent social responses, a re-examination of current
husbandry practice is required to ensure that animals develop in an environment that facilitates
these important suites of interaction and association.
Conclusions: Future directions and new research questions
Mason et al. (2007) argue that zoos should have a “zero tolerance” approach to ARB performance,
however this may be easier said than done. Eradication of ARBs may not be possible in individual
animals whose background (prior to residing in the zoo) may have caused the need for disturbed
behavioral repertories. Change from the top down is one way of ultimately improving the welfare of
captive animals (Maple, 2014) by ensuring that those responsible for the zoo’s management take
responsibility for the care of the animals in their institution, by ensuring species’ care follows the
most current, evidence-based guidelines where appropriate. A sound biological understanding of
species kept by those in positions of authority can have a beneficial effect on husbandry routines,
on staff development and on enclosure planning and design.
Amount of space provided is obviously important to some species, and research has shown that a
biological need to roam can correlate directly with a predisposition to perform ARB (Clubb and
Mason, 2007). However, one should consider that animals do not have boundless freedoms in the
wild (Robinson, 1998) and as such, the quality of space provided in the zoo is much more
important than quantity (Maple, 2007). Here the comparative method can be extremely helpful;
data on time budgets from free-living individuals will provide information on environmental
constraints that influence range sizes and habitat usage, and therefore activity patterns. Zoos can
offer constant climates over time, compared to the seasonality experienced by many species in the
wild state, and therefore there is a trade-off between attempted recreation of a species’ range
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against space that it actually needs to perform important behaviors, or space needed to feel secure
in. Zoos can use functional substitutes (Figure 2) to replicate aspects of the species’ environment
that enable performance of highly-motivated behavior patterns as one way of helping reduce
likelihood of ARB performance.
Figure 2 GOES HERE
Figure 2: Robinson (1998) uses the klipspringer (Oreotragus oreotragus) as an example of a
species hard-wired to perform a behavior with a specific ecological function (vigilance from a high
vantage point) but one that can cope with replication of the functional aspect of its environment
(i.e. provision of a high platform). Photo credit: B Huffman.
The identification of ARB is a useful tool for indicating problematic husbandry and need for
improvement. What is now required, is the use of this information to help the animal long-term by
implementing actual improvements to husbandry that have a measureable, positive, impact on
welfare (Rushen and Mason, 2008). It is evident that enrichment can help alleviate ARB
performance and reduce the animal’s reliance on their performance. Research shows that
subsequently removing environmental enrichment is problematic (Latham and Mason, 2010). As
such, enrichment programs that enable the animals to experience environmental control and
choice, and are stimulating without being frustrating and need to be planned and implemented on
an individual- and species-specific level. Table 2 provides an outline of focused research questions
that, when answered, may help expand our understanding of how evidence-based husbandry can
reduce overall ARB performance across the whole range of zoo-housed taxa.
TABLE 2 GOES HERE
Table 2: Suggested research questions to advance zoo animal welfare, provide evidence for good
husbandry and reduce ARB performance
Case studies that review specific aspects how the animals engage with their environment and the
way this changes with provisioning can tell us ways that behavior patterns can be improved and/or
a more naturalistic time budget be performed (Bashaw et al., 2001; Bashaw et al., 2007; Rose and
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Robert, 2013; Rose et al., 2014b; Rose et al., 2016). Such directed research into individual species
is a clear way of assessing positive welfare, and then disseminating best practice to those able to
influence husbandry standards in other zoos. We agree with the stance of Mason et al. (2007) that
good zoos are determined to tackle ARB in their animal collections, to ultimately enhance welfare
state for species that are maintained. In the decade since their seminal paper, new data that
illuminate species differences in responses to captivity are available to help zoos inform practice.
Novel approaches, including individual assessment of welfare (Whitham and Wielebnowski, 2013)
performed over time on an increasing number of animals will provide a knowledge-bank of how to
manage ARB performance in particular species, along with best practice husbandry guidelines
(EAZA, 2015) that help promote optimal care across zoos and reduce an individual animal’s need
to deviate from a natural time budget and/or behavioral repertoire.
Acknowledgements
Thank you to two anonymous reviewers for their comments and suggestions on the manuscript.
Thank you to Mr. B. Huffman for providing the klipspringer photograph for the article, and for
comments to help with the development of the original paper.
Authorship
The idea for the paper was conceived by the first author, after being approached by the editor of
this Special Edition for this journal. The paper was written by all three authors, under the guidance
of the first author.
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989
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991
992
993
994
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1000
1001
1002
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1004
1005
1006
1007
1008
1009
1010
1011
1012
1013

Table 1. Summary of major risk factors and potential solutions to the development of stereotypic
behavior and ARBs in apes and Old World monkeys.
Species ARB Risk Factor Solution Reference
Macaca
mulatta
Motor Lack of foraging
devices
Reared in individual
housing
Reared in protective
contact
Timid, not bold,
temperament
Give forage
puzzles
Rear in full social
contact
Breed bold
individuals
Gottlieb et al.
(2015)
Proportion of life lived
indoors
Proportion of life lived
indoors when singly
housed
Rear with outdoor
access, in a
social group
Vandeleest et al.
(2011)
Pacing Individual housing at
early age
Time spent house
individually
Nursery rearing
Sex (male bias)
Social housing
Minimize time
spent in isolation
Mother rearing
Lutz et al. (2003)
Rommeck et al.
(2009)
Mixed Indoor rearing Rear with access
outside
Gottlieb et al.
(2013)
Premature artificial
weaning
Maternal deprivation
Natural weaning Prescott et al.
(2012)
Individual or social
housing indoors
House
individually or in
Fontenot et al.
38
1014
1015
1016
1017
1018
1019
1020
1021

social groups with
access to outside
(2006)
Maternal deprivation
and isolation rearing
Mother rearing in
social groups
Harlow (1964)
Cerecocebu
s torquatus
torquatus
Pacing and head
rolling
Housed in relatively
small cage
House in semi-
free ranging
environments
Reamer et al.
(2010)
Gorilla
gorilla gorilla
Mixed Lack of privacy from
viewing public
Use camouflage
nets to screen
windows
Blaney and Wells
(2004)
Pan
troglodytes
Mixed Simply being in
captivity
Maintain wild
populations
Birkett and
Newton-Fisher
(2010)
Maternal deprivation Mother rearing Turner et al.
(1969)
Multiple Hair-pulling
Pacing
Un-natural group size
Wild day range not
matched by captive
housing
Appropriate social
stimuli
Complex physical
environment
Pomerantz et al.
(2013)
39
1022
1023
1024
1025
1026
1027
1028
1029
1030
1031
1032
1033
1034
1035

Table 2: Suggested research questions to advance zoo animal welfare, provide evidence for good
husbandry and reduce ARB performance
Research question How to do Applied benefits
The importance of functional
replicates of key habitat
features, and quantitative
study across all taxa to
systematically investigate
ARB and effects of targeted
enrichment.
Using information on behavioral
ecology, enclosure design can be
fashioned so that integral features of
the exhibit are enrichment to the
individuals that inhabit it, as
behaviors of strong homeostatic or
motivational drive can be easily
performed.
Incorporating the important aspects of
a habitat’s features for species kept
may be easier than overall habitat
replication, and a more logistically-
sound way of creating an evidence-
based zoo environment. Elicitation of
natural behavior. Improved animal
welfare and zoo visitor experience
(and education).
Provision of meaningful
environmental heterogeneity
Design and structure enclosures to
provide habitat variation. For
ectothermic species this should
incorporate heterogeneity of
environmental parameters, notably
heat and light.
Providing opportunities for choice
within a complex captive environment
ensures that anthropomorphic need
perception is mitigated and animals
can select appropriate conditions
based on internal motivation and
need.
Enhanced use of species as
husbandry models to
support the development of
behavioral enrichment/
evidence-based systems for
other animals.
Basic husbandry detail is lacking for
many zoo naïve species. Identifying
potential husbandry models
increases the likelihood of
successful husbandry for unfamiliar
taxa.
Work by Rose et al. (2014a) on “pet”
reptile species suggests the wider
application of knowledge from
common species to those we may be
less familiar with. Awareness of
potential interspecific variation, even
between closely related taxa, is
however required.
Further development of
welfare metrics for specific
species housed.
Meta-analysis of zoo populations of
target species to determine typical
activity patterns and behavioral
repertoires. Use these data to
redesign and re-evaluate enclosure
set-up and enrichment programs.
Identification of reliable, non-invasive
welfare indicators (i.e. behavioral
traits) that enable wider recognition of
an individual’s attempts at coping. E.g.
efficacy of enrichment use for captive
bird ARB may not always be based on
evidence (van Hoek and Ten Cate,
1998). Allows for species-specific
enrichment guidelines to be created as
a means of reducing the chance of
ARB development and performance.
40
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1037
1038
1039
1040

Assessing the role that
anticipation plays in ARB
performance.
Comparison across zoos of how
predictable husbandry routines (e.g.
feeding, cleaning, being “locked
out”) affect daily activity patterns.
Multi-zoo, multi-species studies will
enable causal factors to be
assessed and evaluated.
Building on work of Watters (2014) to
alleviate issues of prescriptive
husbandry regimes on performance of
ARB. Flexibility in husbandry regime
may afford the opportunity for more
naturalistic behavioral repertoires.
Welfare implication of
keeping wide-ranging
species (not the obvious) in
zoos, and the impact of
restricting seasonal
movement patterns.
Problems with long-distance
travelers e.g. sea turtles, salmonids,
Charadriiformes. Building on
research from Clubb and Mason
(2003) and applying into avian and
lower vertebrate taxa.
Use of data to alter enclosure design,
target when enrichment should be
provided and help in the development
of more “robust” individuals that could,
potentially, be better suit for
reintroduction or release programs.
Risk assessment for
identification of ARB
development in specific
species situations.
Comparison of wild data with
surveys on husbandry/management
practices across institutions to
correlate positive behavioral effects
with best practice management
situations.
Deterministic factors (i.e. dietary
provision in ungulates and maternal
deprivation in elephants) will allow for
changes in management to prevent a
welfare problem from developing in
the first instance.
Figure 1: promoting positive welfare in captive wildfowl by maintaining birds in appropriate social
groups and by replicating key habitat features linked to important aspects of behavioral ecology. In
this case, common goldeneye (Buchephala clangula) kept on clean water deep enough to allow
diving and underwater swimming, and in a mixed sex flock that facilitates performance of courtship
display.
41
1041
1042
1043
1044
1045
1046
1047
1048
1049

Figure 2: Robinson (1998) uses the klipspringer (Oreotragus oreotragus) as an example of a
species hard-wired to perform a behavior with a specific ecological function (vigilance from a high
vantage point) but one that can cope with replication of the functional aspect of its environment
(i.e. provision of a high platform). Photo credit: B Huffman.
42
1050
1051
1052
1053
1054
1055