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The Importance of Maintaining Natural
Behaviors in Captive Mammals
M. Elsbeth McPhee and Kathy Carlstead
INTRODUCTION
Behavior, like morphology and physiology, evolves in complex environments to increase an individual’s survival and
reproductive success in its native habitat. Captive mammals,
however, are living in environments widely different from
that in which they evolved. In response, they adjust their behavior to cope with their environment, potentially resulting
in genetic and phenotypic divergence between captive and
wild populations (Darwin ; Price , ; Lickliter
and Ness ; McPhee a, b, ).
These responses can occur on  levels. First, an individual
can change its behavior to meet an immediate specific need,
e.g. conforming to feeding schedules or conspecific groupings. Second, growing up in a captive environment that is
more restrictive than the wild can alter how an animal learns
and change how it responds to future events. These changes
occur within an individual, but build as the animal develops. The third level of response comprises many individual
changes, but is expressed across a population. Within a captive population, certain behaviors will confer greater survivorship on the individuals who express them, e.g. greater
tolerance of loud noises. These behaviors will be passed on
genetically from generation to generation, resulting in a distribution of traits within the captive population that is distinct
from distributions observed in wild populations.
Maintaining natural behaviors in captive-bred mammals is
a top priority for zoo biologists, because all  levels of change
may compromise ex situ and in situ conservation efforts for
endangered mammal species. For an individual animal, the
presence of normal, species-specific behaviors, similar to
those observed in the wild, is one potential indicator that its
needs are being met, its captive environment is optimal, and it
has good health and well-being. In exhibited animals, natural
behavior is also a signal to the zoo visitor that the animal is
a viable representative of its wild counterparts. Visitors who
witness captive animals displaying abnormal behaviors are
more likely to perceive those animals as “unhappy” (McPhee
et al. , unpublished data), and increased aberrant behaviors can detract from the educational message of the exhibit
(Altman ). Such negative experiences with captive animals can potentially cause visitors to reject the concept that
zoos are authorities in the preservation of that species and of
biodiversity in general.
In addition, formation of natural species-specific behaviors during growth and development is necessary for successful reproduction. Reproductive behaviors, such as mate
choice, courtship, mating, and rearing of offspring, are significantly influenced by the captive environment (see Swaisgood and Schulte, chap. , this volume; Thompson, Baker,
and Baker, chap. , this volume). For many mammal species, development of natural reproductive behaviors requires
normal learning experiences during early development and
appropriate socialization throughout development. Therefore, to maintain sustainable captive populations, the effects
of captive conditions on the development of behavior must be
given serious consideration in all captive breeding programs
(Kleiman ; Carlstead and Shepherdson ).
Finally, for captive populations to represent their wild
counterparts accurately, overall trait distributions must be
similar. Captive populations are exposed to selective pressures that, over generations, shape behaviors adaptive to the
captive environment. These pressures alter behavioral expression and trait distribution within a population, resulting in
captive populations that are behaviorally and morphologically distinct from wild populations. The captive population may thus evolve toward one lacking individuals able to
survive in a wild environment, severely limiting the ability
of captive populations to contribute to the recovery of wild
populations.
In this chapter we will discuss the importance of addressing all  levels of behavioral change within the contexts of
individual animal well-being, development of natural reproductive behavior, and behavioral diversity of captive populations, and how these relate to in situ and ex situ conservation efforts.
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the imp orta nce of maintaining natural behaviors in captive mammals
ANIMAL WELL-BEING
An ethical and operational imperative of every zoo is to optimize an animal’s well-being (see Kagan and Veasey, chap. ,
this volume). Psychological well-being is an individual-level
phenomenon, for it depends on how an animal perceives its
own ability to respond to changes in its environment and
react to its constraints. Dawkins (, ) suggests that
determining whether the welfare of animals is good or bad
requires answering  questions: is the animal healthy, and
does it have what it wants? Poor physical health is an obvious sign of poor well-being, but other measures of health are
less straightforward, such as reduced food intake or depressed
immune function. Behavioral scientists are increasingly interested in studying stress responses of captive animals in order
to link animal well-being to animal health.
IS THE ANIMAL HEALTHY? STRESS ASSESSMENT
To keep an animal physiologically and behaviorally healthy,
the demands of stress must be kept within a tolerable range.
Chronic stress is an undisputed cause of poor welfare in captive mammals (Broom and Johnson ). Prolonged periods
of high levels of hypothalamic pituitary-adrenal activity in response to repeated or chronically present stressors may have
costly biological consequences, such as immunosuppression
and disease, atrophy of tissues, decreased reproductive function, or maladaptive behavior (Engel ; Henry ; Bioni
and Zannino ; Blecha ; Elsasser et al. ; Whay
et al. ). Stress can be good or bad for an animal depending on how long the stress lasts, how intensive it is, and how
many options the animal has for responding to its situation
(Ladewig ; McEwan ; Wielebnowski ).
There are few zoo studies, however, that relate actual measurements of stress to consequences for animal health; stress
is often presumed rather than measured, based on coincidental occurrence of precipitating events. For example, Cociu
et al. () reported that Siberian tigers, Panthera tigris altaica, at the Bucharest zoo developed gastroenteritis due to
a failure to adapt to unfamiliar quarters. Also, a persistent
high noise level lasting several months caused by repairs in
an adjacent courtyard was thought to induce gastroenteritis
in some of the tigers. There is more recent direct evidence
for a correlation between elevated corticoids and biological
costs among some zoo-housed species. Carlstead and Brown
() provide evidence that mortality in black rhinoceroses,
Diceros bicornis, and reproductive failure in white rhinoceroses, Ceratotherium simum, are associated with high variability in the secretion of stress hormones (glucocorticoids)
from the adrenal cortex. They interpreted high variability in
fecal corticoids over a one-year collection period as indicating an inability of some rhinoceroses to adapt or maintain
homeostatic levels of adrenal activity.
There is also an association of high average glucocorticoid
concentrations with hair loss in polar bears, Ursus maritimus
(Shepherdson, personal communication), and with conspecific trauma, neoplasia, renal disease, and adrenal cortical
histopathology in clouded leopards, Neofelis nebulosa (Terio
and Wielebnowski, personal communication).
To address the causes and reduce the deleterious effects of
stress on well-being and health, measurement of stress in zoo
animals is necessary. How do we assess stress? A definition of
chronic, or “bad,” stress is “when environmental demands tax
or exceed the adaptive capacity of an organism, resulting in
psychological and biological changes that may place a person
or animal at risk for disease” (Cohen, Kessler, and Underwood
Gordon , ). Thus, to measure stress in zoo animals we
must assess and integrate at least  factors: () environmental conditions and changes, () physiological and behavioral
responses to these changes, and () biological consequences
to health, reproduction, and disease processes. In zoos today,
stress assessment is a rapidly growing field that necessitates
the integration of these biological data collected sequentially on individual animals, for individuals perceive stressors differently as a function of their age, sex, background,
personality, or reproductive condition (Benus, Koolhaas, and
van Oortmerssen ; Suomi ; Mason, Mendoza, and
Moberg ; Cavigelli and McClintock ).
The environmental and social events that cause stress in
captive mammals vary depending on the species. Morgan
and Tromborg () provide an admirable review of factors
that elicit stress responses in captive mammals. These include
sound and sound pressure, olfactory stimulation from predators and chemicals, and space restriction (see also Kagan and
Veasey, chap. , this volume). Unstable social groups (DeVries, Lasper, and Detillion ) or unnaturally high group
densities, denied concealment, removal of scent marks, induced feeding competition, or forced proximity to zoo visitors also cause problems (Glatston et al. ; Hosey and
Druck ; Chamove, Hosey, and Schaetzel ; Thompson
). In a multi-institutional study of  clouded leopards,
Wielebnowski et al. () found that public display, proximity of predators, frequent changing of keepers, and lack of
enclosure height are environmental factors associated with
high levels of fecal corticoids and aberrant behavior. Similarly, black rhinoceroses in enclosures with a large percentage
of the perimeter exposed to public viewing had higher fecal
glucocorticoids than those in enclosures with more restricted
viewing (Carlstead and Brown ).
Responses to stressors may include various combinations
of protective or defensive behaviors and neuroendocrine responses, depending on the stressor (Matteri, Carroll, and
Dyer ; Moberg ). Physiological stress responses
may occur transiently in response to normal situations such
as courtship, copulation, or routine husbandry events, or they
may be more sustained or variable as a result of more difficult
challenges. A primary avenue for measuring stress, therefore,
is to pair changes in behavior with changes in physiological
measures, and then examine the precipitating environmental and/or social events. Measurement of glucocorticoids in
feces and urine has become the primary means of studying
stress responses in zoo animals and wildlife, because the collection method is noninvasive and represents a pooled sample
of corticoid output over a period of several hours (Whitten,
Brockman, and Stavisky ; Möstl and Palme ; Hodges,
Brown, and Heistermann, chap. , this volume). In contrast,
sampling blood for corticoid measurement needs to be conducted more frequently under rigidly controlled conditions
in order to control for the naturally pulsatile excretion of
corticoids and for circadian rhythms. This makes measur-
m. elsbeth mcphee and kathy carlstead
ing basal levels and changes associated with environmental
stressors more difficult.
Behavior is the animal’s “first line of defense” in response to
environmental change; it is what animals do to interact with,
respond to, and control their environment (Mench ).
Therefore, behavioral changes must be monitored when assessing stress in zoo animals. The increased occurrence of
repetitive pacing, aggression, excessive sleep or inactivity, or
fear behaviors can be indicative of stress. In a group of socially housed captive gorillas, Gorilla gorilla gorilla, periods of
social instability were indicated by elevated glucocorticoids,
aggressive displays, and fighting (Peel et al. ). Wielebnowski et al. () found that elevated glucocorticoids in
clouded leopards correlated with fur plucking, extensive pacing, and hiding behavior. A singly housed male orangutan,
Pongo spp., had higher glucocorticoid levels on days when the
keepers recorded his temperament as being “upset” and he
refused to shift between enclosures (Carlstead , unpublished data). In a zoo-housed giant panda, Ailuropoda melanoleuca, there was a positive association between glucocorticoids, locomotion, and door-directed scratching behavior
and loud noise levels (Owen et al. ).
Conversely, the frequent occurrence of positive and/or
natural behaviors may indicate low levels of stress and, presumably, good welfare. Leopard cats, Felis bengalensis, living
in virtually barren cages had chronically elevated glucocorticoids and high levels of stereotypic pacing that decreased
dramatically when they were given the opportunity to hide
or conceal themselves in newly provided complex furnishings and vegetation. They also increased the amount of time
spent exploring their cages (Carlstead, Brown, and Seidensticker ). Falk (personal communication) reported that,
at one zoo, opening the shift doors for polar bears and giving
them the choice to go inside or outside greatly reduced stereotypic pacing. Individual white rhinoceroses that keepers
assess as being most adapted to their captive environment
based on how “friendly” they are toward the keeper have
lower mean glucocorticoids than conspecifics who seem less
relaxed around keepers (Carlstead and Brown ).
DOES THE ANIMAL HAVE WHAT IT WANTS?
In zoos, absence of stress and abnormal behaviors are, by
themselves, insufficient criteria to ensure animal well-being.
Animals are motivated to perform behaviors (see Shepherdson, chap. , this volume), and animal welfare science seeks to
identify which behaviors the animal wants/needs to do most
(e.g. hunting, foraging, swimming). Captive mammals should
also be active at levels similar to those in the wild (Kagan and
Veasey, chap. , this volume). Thus, they need to be able to
carry out highly motivated behaviors, especially those that
result in a level of behavioral proficiency that supports the
goals of the program for which they were raised (e.g. reintroduction, social living, captive breeding, program animal
docile to humans, or exhibit animal displaying normal behavior). Motivations change with the season and reproductive condition; e.g. an American black bear, Ursus americanus,
had a seasonal pattern of stereotypic pacing where the pacing changed temporally and spatially depending on whether
it was the mating season or the prewintering season. Carl-
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stead and Seidensticker () interpreted this result to indicate a change in what the bear wanted—mating or foraging
opportunities.
Two of the most common approaches to determine whether
an animal has what it wants are () using environmental modifications and enrichment to reduce experimentally negative
behaviors such as stereotypy, aggression, and excessive inactivity, and to increase activity levels and behavioral diversity, and () choice tests through which animals may indicate
which behaviors they are most highly motivated to perform.
One explanation for negative behaviors such as stereotypies
is that appetitive motivation to seek something missing in the
environment causes the animal to channel motivation toward
repetitive locomotion (reviewed in Mason and Latham ;
see Shepherdson, chap. , this volume). In other words, the
animal cannot find an outlet for its desired behavior. As an
example, feeding in the wild constitutes a large portion of
some species’ activity budget. Foraging and hunting are processes that include searching, acquiring (harvesting or capturing and killing), and consuming food items (Lindburg
). Captive animals, however, rarely have opportunities to
do anything but consume, and often that is a compromised
experience, as food is reduced from a complex (e.g. an intact
prey item) to an overly simple form (e.g. preprocessed meat).
In such cases, enrichment in the form of provisioning with
whole carcasses increases handling time of food and reduces
time spent in stereotypic pacing (ibid.; McPhee ).
Choice tests can suggest what the animal “wants” to be
doing for pleasure, comfort, or satisfaction and have demonstrated that animals usually prefer challenges and engagement
over passive rewards (Mench ). Animals of many species
prefer to work for food, such as running a maze or pushing a
lever, as opposed to getting food for free. Likewise, they prefer to explore novel environments and objects.
Modifications to animals’ environments or changes in
feeding methods frequently reduce negative behaviors and
increase activity and behavioral diversity (for a review, see
Swaisgood and Shepherdson  and Shepherdson, chap.
, this volume). Wiedenmayer () hypothesized that stereotypic digging develops in captive Mongolian gerbils, Meriones unguiculatus, because the stimuli that normally cause the
animal to cease digging were lacking in the captive environment. He kept young gerbils on a wood-chip substrate with
access to an artificial burrow and found less digging behavior
than in gerbils that were able to dig in a dry, sandy substrate
which was incapable of supporting a burrow.
In many captive species, stereotypies occur mainly before
feeding time, when the animal is motivated to perform food
acquisition behaviors such as foraging or hunting. Winkelstraeter () describes a female ocelot, Leopardus pardalis, that ran in a circular path before feeding. Similarly, Geoffroy’s cats, Felis geoffroyi, paced for  to  hours before feeding
time (Carlstead ). Stereotypic behaviors in large felids decrease with the provisioning of intact prey items, while foodhandling time and other consumptive behaviors increase (e.g.
crouch, stalk, pounce, leap, swipe, bite, hold, eat) (McPhee
; Bashaw et al. ). An American black bear paced less
and explored/foraged more before feeding time when food
was scattered throughout its enclosure (Carlstead, Seidensticker, and Baldwin ). Gould and Bres () had some
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the imp orta nce of maintaining natural behaviors in captive mammals
success in reducing regurgitation behavior in captive gorillas
by feeding browse, which increased time spent handling and
ingesting food. Such studies can be interpreted as meaning
that animals benefit from the opportunity to “work” for their
food (Markowitz ).
Another fundamental question is whether an animal has
as much space as it wants or needs in a zoo enclosure. For
carnivores and other wide-ranging species, home range size
predicts the level of pacing in captivity (Clubb and Mason
). With primates, generally the smaller the cage, the more
some individuals perform stereotypies (Paulk, Dienske, and
Ribbens ; Prescott and Buchanan-Smith ). By increasing the size of the area available to an animal, the behavior can sometimes be eliminated or altered (Draper and
Bernstein ; Clarke, Juno, and Maple ).
Exactly how much space an animal needs is unclear, particularly because the critical factor for well-being is often the
quality of the space (Berkson, Mason, and Saxon ). Polar
bears have the largest home ranges of all carnivores in the wild
and presumably need the most space in zoos—more space, in
fact, than can be provided by any zoo. Shepherdson’s recent
multi-institutional study of polar bear stereotypy found that
enrichment and training is highly negatively correlated with
time spent in stereotypy, implying that giving bears something to do continually can be compensation for lack of space
(Shepherdson, personal communication). Perkins () and
Wilson () found that cage size was not as important for
stimulating higher levels of activity in groups of zoo-housed
great apes (gorillas and orangutans) as was the number and
type of furnishings. Odberg () compared the behavior of
bank voles, Myodes glareolus, in small, rich environments and
in large, sparse ones, and found less stereotypic jumping in
the former. Similarly, spatial confinement was not a causal
factor of stereotypies in Mongolian gerbils (Wiedenmayer
). Such evidence lends credence to Hediger’s () statements that the quality of a confined animal’s space is more
important than the quantity.
Choice tests are common in animal welfare research of
intensive farming practices to determine how much effort
animals are willing to expend to achieve access to opportunities for preferred activities. Dawkins () has used a consumer demand model derived from economic theory that
requires animals to work to acquire commodities. For example, Mason, Cooper, and Clarebrough () found that
mink, Mustela vison, expend more energy pressing a weighted
door to acquire access to a swimming pool than to gain access to toys, novel objects, or alternative nest sites. When
deprived of pool access they exhibited corticoids elevated to
a level similar to the corticoid response when they are food
deprived. The authors concluded that farmed mink are still
highly motivated to perform aquatic activities despite being
bred in captivity without access to pools of water for  generations.
Choice test experiments are not commonly used with zoo
animals, because standardizing environments sufficiently to
offer  equal choices is difficult. However, studies of space
utilization that divide enclosures into grids can assess animal preferences to some degree, particularly when behavior
is also assessed. For example, Mallapur, Qureshi, and Chellam () found that almost all  leopards, Panthera par-
dus, in Indian zoos used the edge zone of their enclosure for
stereotypic pacing and the “back” zone, farthest from visitors, for resting.
Of additional interest for future research are the individual
differences when using operant conditioning to train captive
animals: learning and performing behaviors could be an indication of willingness to work for food rewards or social interaction with the keeper (see Mellen and MacPhee, chap.
, this volume). Certainly, there are individuals who choose
not to be trained, or do so only for their most highly valued
rewards.
BEHAVIORAL DEVELOPMENT AND REPRODUCTION
Maintaining natural reproductive behaviors in captive-bred
animals is vital to the establishment of self-sustaining captive populations and maintaining genetic diversity within
those populations. Historically, however, many captive mammals have reproduced with difficulty or not at all (Wielebnowski ). Common problems include inability to court
and choose mates, copulate successfully, or rear viable offspring, often due to a lack of normal species-specific interactions with the environment as an animal matures. As with
animal welfare, such developmental problems are observed
at the individual level.
Interactions between the developing organism and its
environment start before birth, since the hormonal state of
the mother affects the uterine environment of the growing
fetus. There are numerous reports of the effects of stress experienced by mothers during pregnancy on the behavior of
their offspring, including increases (Ader and Blefer )
or decreases (Thompson, Watson, and Charlsworth )
in emotionality in a novel environment (open field), alterations of exploratory behavior in rats (Archer and Blackman
), and reductions in attack and threat behavior in male
offspring in mice (Harvey and Chevins ). Male offspring
of mother rats stressed daily in the last week of gestation
showed reductions in attempted copulations and ejaculation
responses as adults (Ward ). Such studies imply that prenatal stressors specific to a captive environment can cause
postnatal behavioral changes that reduce reproductive viability of offspring.
In most mammals, the mother-infant relationship is
critical to the future development of offspring, affecting future
defensive responses and reproductive behavior (Cameron
et al. ). Subtle aspects of the parent-infant or juvenilepeer relationship may affect later sexual preferences and competence, and researchers speak of an extended period of socialization occurring during infant and juvenile stages (Aoki,
Feldman, and Kerr ). A disturbed mother-infant relationship may deprive the young animal of specific stimulation essential for the development of normal emotional regulation,
social interaction, and complex goal-directed behaviors, in
particular, maternal and sexual behaviors. Deprivation of
maternal licking when pups are young has been shown to affect the timing of sexual behavior patterns in male rats when
grown; intromissions were more slowly paced and the rats
took longer to ejaculate (Moore ).
Relationships with peers are also important, especially for
great apes. Maple and Hoff () found that young gorillas
m. elsbeth mcphee and kathy carlstead
maintained with little or no conspecific contact are often sexually dysfunctional as adults. Captive female chimpanzees,
Pan troglodytes, are better mothers when they have social experience with nonrelated infants or other mothers with infants (Hannah and Brotman ).
As an animal matures in captivity, many elements influence it that are unique to the captive environment. Close
contact with humans can produce a range of behavioral characteristics not found in a wild-reared animal, depending on
when it occurs during the animal’s development and how
long it is sustained. The most significant effects of human
contact on overall behavior likely occur as a result of contact
early in life in lieu of caregiving by the natural mother (i.e.
hand rearing) (see also Thompson, Baker, and Baker, chap.
, this volume). In a study of western lowland gorillas, Ryan
et al. () found that mother-reared females had more offspring and were more likely to become successful mothers
than hand-reared females.
Early socialization with humans can affect species-specific
social skills in both positive and negative ways. Among ungulates with precocial young, filial imprinting, in which the
young learn to follow the mother (rather than objects and individuals that do not resemble the mother), occurs within the
first day or two of life (for reviews see Bateson ; Hogan
and Bolhuis ). Guinea pigs, Cavia porcellus, also exhibit
characteristics of filial imprinting (Sluckin ; Hess ).
Removing a young animal from the mother during this sensitive period may result in following responses being elicited
by human caregivers, as is commonly seen in sheep and goats,
but has also been reported in the American bison, Bison bison,
zebra, Equus spp., African buffalo, Syncerus caffer, mouflon,
Ovis musimon, and vicuña, Vicugna vicugna (see Hediger
). Mellen and MacPhee (chap. , this volume) recommend caution in training young male ungulates, because as
they mature they tend to show aggression toward humans.
Ideally, captive-born mammals should be socialized with humans only to the point where they have minimal fear of humans (tameness) but still recognize them as heterospecifics.
Many reproductive deficiencies derive from an inappropriate developmental environment, while others occur through
lack of opportunities in captivity. In the wild, many mammals
can choose their mate based on cues ranging from chemical
odors to complicated courtship displays. Based on such cues,
wild individuals tend to choose a mate such that inbreeding
is decreased, pathogen resistance is increased, and ultimately,
survival and reproductive success of offspring are maximized
(Grahn, Langefors, and von Schantz ). Many species have
evolved mechanisms by which they choose mates that are genetically dissimilar, which reduces the risk of inbreeding
(Blouin and Blouin ) and increases the ability of offspring
to resist disease. House mice, Mus musculus, prefer mates
that are genetically dissimilar at the major histocompatibility complex (MHC), a suite of genes responsible for immune
function, thus conferring increased immune response and
disease resistance in their offspring (Penn and Potts ).
Grahn, Langefors, and von Schantz () suggest that allowing greater mate choice in captive animals might increase
disease resistance in captive populations through increased
diversity of the MHC. Specifically, they suggest allowing cap-
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tive males to display for females and using female reactions
to guide breeding decisions.
Captive mammals, however, are not usually given the opportunity to assess multiple potential mates and ultimately
choose an individual suitable to them. Indeed, little is known
about how mate preferences develop or are lost in captive
populations. For example, species differ in whether familiarity is a good or a bad feature, and in some, the introduction
of an unfamiliar individual as a mate results in high levels of
aggression. Yamada and Durrant () found that clouded
leopards need to be paired while still sexually immature; in
pairs established later, males show extreme aggression toward
females, often resulting in serious or fatal injuries. Female
kangaroo rats, Dipodomys heermanni arenae, were less aggressive toward and more responsive to familiar males with
whom they had prior experience (Thompson ). By contrast, cheetah, Acinonyx jubatus, and white rhinoceroses are
anecdotally known to be more likely to breed with newly introduced, unfamiliar mates.
BEHAVIORAL DIVERSITY
Animal managers must also be aware of how small, individual
changes affect behavioral trait expression at the population
rather than the individual level. Selection in captivity can affect the expression of behavioral traits in multiple ways; however, the selective pressures associated with captivity are vastly
different from those in the wild environments in which species have evolved (Hediger ; Price ; Frankham et al.
; Soulé ; Soulé et al. ; Price ; Seidensticker
and Forthman ). Captivity can thus impose novel selective pressures—either intentionally or inadvertently (Price
, ; Endler )—and, over generations, result in
changes in important life history and behavioral traits that
affect functional relationships between behavioral, morphological, and physiological traits (McDougall et al. ). Understanding and identifying the ultimate mechanisms behind
behavioral change can be difficult, because different selective
pressures do not occur in isolation of one another. One trait
may experience relaxed selection, while another experiences
directional. The overall expression of traits is therefore the
result of complicated synergistic effects. For the purposes of
this chapter, we will focus on directional and relaxed selection.
Directional selection occurs when the expression of traits
at one end of the distribution is favored (Endler ). In this
case, mean trait expression will shift, but variance around the
mean will not necessarily change (fig. .a). For example,
time spent foraging is a trade-off with predator avoidance
for many wild species. More time foraging means more food,
but it also means higher predation risk. On the other hand,
reduced foraging time might decrease probability of predation, but the animal will have fewer resources than its bolder
counterparts. In the captive environment, that trade-off does
not exist. Some animals that are given foraging opportunities
may increase the amount of time spent foraging—and as a
result have healthier offspring and higher reproductive success than individuals who continued to balance foraging and
vigilance. In this case the trait foraging time has been pushed
in an increasing direction.
308
the imp orta nce of maintaining natural behaviors in captive mammals
A
B
Fig. 25.1. Directional and relaxed selection. The solid curve represents
the original distribution of a trait; the dashed curve represents how
the distribution changes due to either directional (A) or relaxed (B)
selection. With directional selection, the mean shifts, but the shape
of the distribution does not change; with relaxed selection, the mean
remains the same, but the distribution flattens out, including more
values at either extreme.
Relaxed selection can occur when captive conditions
permit expression of certain behavioral traits that otherwise
would have been selected against in the wild, resulting in an
increase in genotypic and phenotypic trait variability (Endler ; fig. .b). Consider the time necessary to respond
to a predator. In the wild, animals have limited time to detect a predator and flee. In a captive environment, however,
there is typically no predation and individuals can respond
immediately, or never, to perceived threats with no effect on
reproductive success. In this case, relaxed selective pressures
in the captive environment result in an increase in variance
in response time.
In one of the few investigations of population-level behavioral processes affecting captive mammals, McPhee (a,
b, ) tested for directional and relaxed selection in
captive-bred oldfield mice, Peromyscus polionotus subgriseus,
and found that behavioral and morphological divergence from
the wild population increased with generations in captivity,
primarily due to relaxed selection. Trait variance increased significantly for burrow/refuge use, activity level, response time
to predators, and skull shape. To our knowledge, this is the
only explicit test of these hypotheses in mammals. We recommend more research in this area to identify interspecific and
trait-specific patterns, as well as linkages between traits.
Initially, these increases in behavioral trait variance may
seem counter to the large body of literature that shows that,
with generations in captivity, genetic variance decreases. Two
views can potentially resolve this difference. First, phenotypes may be the primary trait on which selection acts (WestEberhard ), and minor genetic changes can result in profound phenotypic changes, which are then selected for (or
not). Second, reduced genetic variance resulting from inbreeding is not natural selection—it is the reduction of genetic variance based on what genes are available. Selection
then acts on the phenotypic expressions that result from in-
breeding, a process that may ultimately appear to reduce genetic variance.
Artificial selection, be it directional or relaxed, can be
intentionally or inadvertently imposed. The most common
form of intentional artificial selection is domestication (Price
). Humans have attempted, but failed, to domesticate
many species. Not all animals are amenable to domestication, because certain behavioral characteristics are more favorable for domestication than others. Easily domesticated
species generally live in large, hierarchical social groups in
which the males affiliate with female groups, and mating is
promiscuous. Young are precocial and experience a sensitive
imprinting period during development. They are also generally adapted to a wide range of environments and dietary
habits rather than to highly specialized conditions (ibid.).
Species targeted for domestication are subjected to strong
selective pressures designed to produce a certain outcome,
e.g. increased milk production in dairy cows or long, pointed
snouts in rat-hunting dogs; but many behavioral changes in
domesticated populations are the indirect consequence of
selection for other morphological and/or physiological attributes. For example, in Belyaev’s famous selection experiments with silver fox, Vulpes vulpes, animals selected over
generations exclusively for tameness also exhibited a shift
from one to  annual estrous cycles (Belyaev and Trut )
as well as phenotypic traits such as floppy ears and curly tail
that are typical of domesticated dog species (Trut ). Although nondomestic captive populations do not undergo
such strong intentional selection, they do experience unintentional selective pressures. For example, temperament in
captive mammals is likely shaped by directional selection
(Arnold ; Frankham et al. ; McDougall et al. ).
In captivity, docile individuals are easier to handle, transport, and medicate than their more aggressive counterparts.
In a human-controlled environment, docility might translate
into better survival and reproduction, which could lead to
unconscious artificial selection for docility and tractability
in mammals—selection that may eventually make captive
populations divergent from wild populations. On the other
hand, Kunzl et al. () compared behavior and physiological responses of domestic guinea pigs, Cavia aperea f. porcellus, wild-caught cavies, and captive-bred cavies, Cavia aperea,
bred with no purposeful selection. There were no significant
differences between the wild-caught animals and those bred
in captivity for  generations, suggesting that purposeful
selection for specific traits may be necessary to produce domesticated animals.
CONSERVATION IMPLICATIONS
Maintaining natural behaviors in captive-bred animals is vital
to the success of conservation efforts that rely on those animals, such as zoo education and reintroduction of captivebred animals into their native habitat.
VISITOR EXPERIENCE
Maintaining good animal welfare is important for not only
the individual animal, but also the zoo visitor. Zoos often
justify the exhibition of exotic species by highlighting the
m. elsbeth mcphee and kathy carlstead
zoo’s and the species’ educational value. A zoo is likely the
only opportunity most people have to see such animals live,
and most of a visitor’s education while at a zoo comes from
watching the exhibited animals (see Routman, Ogden, and
Winsten, chap. , this volume).
Zoo visitors often base their evaluation of an animal’s
health and “happiness” on observed behavior (Wolf and Tymitz ). In general, visitors tend to be more engaged in front
of an exhibit with an active animal (Altman ; Margulis,
Hoyos, and Anderson ). When that activity is the display
of obviously repetitive and abnormal behaviors, however, visitors perceive animals to be “unhappy” and “bored” (McPhee
, unpublished data).
Through nature documentaries and other media sources,
visitors are coming into zoos with more background information than ever before, e.g. knowledge of how animals in
the wild behave. This knowledge, however, can create false
expectations. Nature programs often show carnivores capturing and killing prey. Yet, when visitors see a captive carnivore,
it is often sleeping (a very natural behavior), and they may
think it is “bored” and has “nothing to do” (Wolf and Tymitz
; McPhee , unpublished data).
Exhibit type also influences visitor perceptions of natural
behavior. McPhee et al. () surveyed over  Brookfield Zoo (Brookfield [Chicago], Illinois) visitors in front of
 exhibits—an outdoor barren grotto, an outdoor vegetated
grotto, an indoor immersion exhibit, and an outdoor traditional cage—and found that visitors were more likely to
perceive animals observed in more naturalistic enclosures as
behaving naturally and thus being “happy,” compared with
animals in traditional cagelike enclosures. Perceptions of animal well-being also strongly affected the educational power
of a zoo exhibit. Visitors that observe behaviorally healthy
animals are more likely to walk away with an appreciation
for that species’ biological significance and need for conservation. These data suggest that, ultimately, an animal’s behavior is the most powerful communicator of that individual’s
health and well-being as well as its natural history and conservation value.
REINTRODUCTION
Though most zoo animals will spend their entire lives as captive representatives of their wild counterparts, a very small
percentage of individuals are targeted for release into their
native habitat. Due to changes in important life history and
behavioral traits, however, individuals from an established
captive population are often at a disadvantage upon reintroduction. Evaluation of reintroduction programs indicates that
many deaths of reintroduced animals are due to behavioral
deficiencies (Kleiman ; Yalden ; Miller, Hanebury,
and Vargas ; Biggins et al. ; Britt, Katz, and Welch
). When golden lion tamarins, Leontopithecus rosalia,
were first reintroduced into the coastal rain forests of Brazil,
captive-born animals had deficient locomotor skills; they
could not orient themselves spatially; and they were unable
to recognize natural foods, nonavian predators, and dangerous nonpredaceous animals (Kleiman et al. ; Stoinski and
Beck ). Similarly, in Madagascar, reintroduced blackand-white ruffed lemur, Varecia variegata variegata, failed
309
to avoid predators, find food, negotiate a complex arboreal
environment, and recognize appropriate habitat (Britt, Katz,
and Welch ). In , all known wild black-footed ferrets,
Mustela nigripes, were brought into captivity for breeding and
eventual release of offspring. The initial releases of captivebred ferrets resulted in high mortality due to predation, suggesting antipredator deficiencies (Reading et al. ).
Since many of these problems stem from the fact that the
animals developed and matured in a captive environment,
such behavioral problems might be eliminated by training
animals targeted for reintroduction for certain skills before
release. Most work in this area has been done with predator response behaviors. For juvenile prairie dogs, Cynomys
ludovicianus, prerelease training consisted of exposure to
either a live black-footed ferret, a live prairie rattlesnake,
Crotalus viridis, or a mounted red-tailed hawk, Buteo jamaicensis. All exposures were coupled with the appropriate
conspecific alarm call, but there was no aversive stimulus
associated with the predator presentation. This training was
sufficient to enhance survival for at least the first year postrelease (Shier and Owings ). Similarly, captive-bred Siberian polecats, Mustela eversmanni, exposed to predator
models (e.g. great horned owl, Bubo virginianus, and badger, Taxidea taxus) coupled with mildly aversive stimuli,
exhibited heightened antipredator responses (Miller et al.
). McLean, Lundie-Jenkins, and Jarman () trained
hare-wallabies, Lagorchestes hirsutus, to be cautious in the
presence of new predators. Prerelease training, especially in
orientation and locomotor behavior, for golden lion tamarins was not as effective as hoped in increasing survival
(Kleiman ; Beck ; Beck et al. ). However, pairing captive-bred individuals with experienced wild-caught
animals did increase the reintroduced animals’ survival rate
(Kleiman ).
Prerelease training can also be used to establish hunting
and foraging behaviors. For example, red wolves, Canis rufus,
were exposed to carcasses and live prey before release, and
swift foxes, Vulpes velox, were given natural foods in the form
of road-killed prey (ungulates and beavers) and chicks from a
local hatchery (USFWS  and Scott-Brown, Herrero, and
Mamo , as cited in Kleiman ). Black-footed ferrets
that had prerelease conditioning with prey were more efficient
at locating and killing prey than those without prey experience (Vargas and Anderson ).
At the population level, understanding how selection has
altered the distribution of key behavioral traits within the
population may allow reintroduction biologists to compensate for the observed changes. If the distribution of a trait or
traits has shifted significantly, the proportion of individuals
in a population that exhibits natural behaviors will also shift.
Mortality will then increase in the release population, because
fewer individuals will exhibit behaviors adapted for the wild
environment. If a program’s goal is to release  individuals,
the question becomes how many need to be released such that
 individuals will fall within the natural behavioral range?
To address this question, McPhee and Silverman () developed the concept of the release ratio, a calculation that
uses trait variances in release and wild populations to determine the number of release individuals needed such that the
targeted number of individuals exhibits natural behaviors.
310
the imp orta nce of maintaining natural behaviors in captive mammals
For example, McPhee’s (a, b, ) behavioral and
morphological measurements of oldfield mice showed that
various traits, such as time to burrow and time in a refuge
after having been exposed to a predator, exhibited significant increases in variance. Thus, if a representative sample
of the captive population were released into the wild, there
would be more individuals in the tails of trait distributions
than would be seen in a wild population, resulting in a higher
mortality rate than would otherwise be expected. Based on
these data, McPhee and Silverman () calculated release
ratios of about . for the oldfield mouse, which means that
for every  mice targeted to exhibit wild-type behaviors,
 individuals need to be released.
CONCLUSION
In this chapter we highlighted  areas in which understanding and maintaining captive mammals’ natural behavior is
key to the success of propagation programs. We commonly
see behavioral change in captive and captive-bred mammals,
and these changes can occur on a number of levels. First, individuals adapt their behavior to captive conditions. Chronic
or repeated stress due to inappropriate environmental conditions may result in poor health for a captive mammal. In
addition, animals need to be able to carry out a diversity
of species-appropriate behaviors. Thus, zoos and aquariums
have a responsibility to promote a range of natural behaviors through appropriate exhibit design, husbandry, and enrichment programs. Second, as an individual develops and
matures, behaviors emerge that are the result of interactions
between the individual’s genetic makeup and its captive environment. In some cases, such changes can have strong negative effects on an individual’s ability to reproduce successfully,
thus affecting the probability of maintaining a sustainable ex
situ population. Finally, captivity can exert directional or relaxed selective pressures on behaviors that will affect the frequencies of those behaviors in future generations. Therefore,
as individual behavior shifts, the distribution of traits within
a population will also shift over generations.
One of the primary missions of zoos is conservation education through animal exhibitry, outreach programs, on-site
tours and courses, and exhibit graphics (Hutchins, Willis, and
Wiese ; Routman, Ogden, and Winsten, chap. , this
volume). Behaviorally healthy captive-bred animals enhance
in situ conservation primarily by educating the public about
and instilling an appreciation for the importance of conservation. For many visitors, the zoo setting will be their only
opportunity to see most species of wildlife. What that visitor
takes away from the experience in terms of appreciation for
the species and understanding of its natural history is largely
dependent on what the visitor experiences—an animal in a
barren cage displaying aberrant behavior or a behaviorally
healthy animal in a naturalistic enclosure, doing what it does
naturally in the wild.
Another conservation imperative of zoos is providing viable animals for reintroduction into native habitat. If captive
breeding is to be a successful conservation tool, we must understand how captivity affects behavior developmentally and
genetically, and how we can counter those effects if they are
deleterious. More immediately, however, we need to maintain
natural behaviors in captive animals because it is ethically imperative from the perspective of animal well-being.
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