The Importance of Maintaining Natural Behaviors in Captive Mammals M

25 The Importance of Maintaining Natural Behaviors in Captive Mammals M. Elsbeth McPhee and Kathy Carlstead

et al. , unpublished data), and increased aberrant behav- INTRODUCTION iors can detract from the educational message of the exhibit Behavior, like morphology and physiology, evolves in com- (Altman ). Such negative experiences with captive ani- plex environments to increase an individual’s survival and mals can potentially cause visitors to reject the concept that reproductive success in its native habitat. Captive mammals, zoos are authorities in the preservation of that species and of however, are living in environments widely diff erent from biodiversity in general. that in which they evolved. In response, they adjust their be- In addition, formation of natural species- specifi c behav- havior to cope with their environment, potentially resulting iors during growth and development is necessary for suc- in genetic and phenotypic divergence between captive and cessful reproduction. Reproductive behaviors, such as mate wild populations (Darwin ; Price , ; Lickliter choice, courtship, mating, and rearing of off spring, are sig- and Ness ; McPhee a, b, ). nifi cantly infl uenced by the captive environment (see Swais- Th ese responses can occur on  levels. First, an individual good and Schulte, chap. , this volume; Th ompson, Baker, can change its behavior to meet an immediate specifi c need, and Baker, chap. , this volume). For many mammal spe- e.g. conforming to feeding schedules or conspecifi c group- cies, development of natural reproductive behaviors requires ings. Second, growing up in a captive environment that is normal learning experiences during early development and more restrictive than the wild can alter how an animal learns appropriate socialization throughout development. Th ere- and change how it responds to future events. Th ese changes fore, to maintain sustainable captive populations, the eff ects occur within an individual, but build as the animal devel- of captive conditions on the development of behavior must be ops. Th e third level of response comprises many individual given serious consideration in all captive breeding programs changes, but is expressed across a population. Within a cap- (Kleiman ; Carlstead and Shepherdson ). tive population, certain behaviors will confer greater survi- Finally, for captive populations to represent their wild vorship on the individuals who express them, e.g. greater counterparts accurately, overall trait distributions must be tolerance of loud noises. Th ese behaviors will be passed on similar. Captive populations are exposed to selective pres- genetically from generation to generation, resulting in a dis- sures that, over generations, shape behaviors adaptive to the tribution of traits within the captive population that is distinct captive environment. Th ese pressures alter behavioral expres- from distributions observed in wild populations. sion and trait distribution within a population, resulting in Maintaining natural behaviors in captive-bred mammals is captive populations that are behaviorally and morphologi- a top priority for zoo biologists, because all  levels of change cally distinct from wild populations. Th e captive popula- may compromise ex situ and in situ conservation eff orts for tion may thus evolve toward one lacking individuals able to endangered mammal species. For an individual animal, the survive in a wild environment, severely limiting the ability presence of normal, species-specifi c behaviors, similar to of captive populations to contribute to the recovery of wild those observed in the wild, is one potential indicator that its populations. needs are being met, its captive environment is optimal, and it In this chapter we will discuss the importance of address- has good health and well-being. In exhibited animals, natural ing all  levels of behavioral change within the contexts of behavior is also a signal to the zoo visitor that the animal is individual animal well-being, development of natural repro- a viable representative of its wild counterparts. Visitors who ductive behavior, and behavioral diversity of captive popu- witness captive animals displaying abnormal behaviors are lations, and how these relate to in situ and ex situ conserva- more likely to perceive those animals as “unhappy” (McPhee tion eff orts.

303 304 the importance of maintaining natural behaviors in captive mammals

stress on well-being and health, measurement of stress in zoo ANIMAL WELL-BEING animals is necessary. How do we assess stress? A defi nition of An ethical and operational imperative of every zoo is to op- chronic, or “bad,” stress is “when environmental demands tax timize an animal’s well-being (see Kagan and Veasey, chap. , or exceed the adaptive capacity of an organism, resulting in this volume). Psychological well- being is an individual- level psychological and biological changes that may place a person phenomenon, for it depends on how an animal perceives its or animal at risk for disease” (Cohen, Kessler, and Underwood own ability to respond to changes in its environment and Gordon , ). Th us, to measure stress in zoo animals we react to its constraints. Dawkins (, ) suggests that must assess and integrate at least  factors: () environmen- determining whether the welfare of animals is good or bad tal conditions and changes, () physiological and behavioral requires answering  questions: is the animal healthy, and responses to these changes, and () biological consequences does it have what it wants? Poor physical health is an obvi- to health, reproduction, and disease processes. In zoos today, ous sign of poor well- being, but other measures of health are stress assessment is a rapidly growing fi eld that necessitates less straightforward, such as reduced food intake or depressed the integration of these biological data collected sequen- immune function. Behavioral scientists are increasingly inter- tially on individual animals, for individuals perceive stres- ested in studying stress responses of captive animals in order sors diff erently as a function of their age, sex, background, to link animal well- being to animal health. personality, or reproductive condition (Benus, Koolhaas, and van Oortmerssen ; Suomi ; Mason, Mendoza, and Moberg ; Cavigelli and McClintock ). IS THE ANIMAL HEALTHY? STRESS ASSESSMENT Th e environmental and social events that cause stress in To keep an animal physiologically and behaviorally healthy, captive mammals vary depending on the species. Morgan the demands of stress must be kept within a tolerable range. and Tromborg () provide an admirable review of factors Chronic stress is an undisputed cause of poor welfare in cap- that elicit stress responses in captive mammals. Th ese include tive mammals (Broom and Johnson ). Prolonged periods sound and sound pressure, olfactory stimulation from preda- of high levels of hypothalamic pituitary- adrenal activity in re- tors and chemicals, and space restriction (see also Kagan and sponse to repeated or chronically present stressors may have Veasey, chap. , this volume). Unstable social groups (De- costly biological consequences, such as immunosuppression Vries, Lasper, and Detillion ) or unnaturally high group and disease, atrophy of tissues, decreased reproductive func- densities, denied concealment, removal of scent marks, in- tion, or maladaptive behavior (Engel ; Henry ; Bioni duced feeding competition, or forced proximity to zoo visi- and Zannino ; Blecha ; Elsasser et al. ; Whay tors also cause problems (Glatston et al. ; Hosey and et al. ). Stress can be good or bad for an animal depend- Druck ; Chamove, Hosey, and Schaetzel ; Th ompson ing on how long the stress lasts, how intensive it is, and how ). In a multi- institutional study of  clouded leopards, many options the animal has for responding to its situation Wielebnowski et al. () found that public display, prox- (Ladewig ; McEwan ; Wielebnowski ). imity of predators, frequent changing of keepers, and lack of Th ere are few zoo studies, however, that relate actual mea- enclosure height are environmental factors associated with surements of stress to consequences for animal health; stress high levels of fecal corticoids and aberrant behavior. Simi- is oft en presumed rather than measured, based on coinciden- larly, black rhinoceroses in enclosures with a large percentage tal occurrence of precipitating events. For example, Cociu of the perimeter exposed to public viewing had higher fecal et al. () reported that Siberian tigers, Panthera tigris al- glucocorticoids than those in enclosures with more restricted taica, at the Bucharest zoo developed gastroenteritis due to viewing (Carlstead and Brown ). a failure to adapt to unfamiliar quarters. Also, a persistent Responses to stressors may include various combinations high noise level lasting several months caused by repairs in of protective or defensive behaviors and neuroendocrine re- an adjacent courtyard was thought to induce gastroenteritis sponses, depending on the stressor (Matteri, Carroll, and in some of the tigers. Th ere is more recent direct evidence Dyer ; Moberg ). Physiological stress responses for a correlation between elevated corticoids and biological may occur transiently in response to normal situations such costs among some zoo-housed species. Carlstead and Brown as courtship, copulation, or routine husbandry events, or they () provide evidence that mortality in black rhinoceroses, may be more sustained or variable as a result of more diffi cult Diceros bicornis, and reproductive failure in white rhinocer- challenges. A primary avenue for measuring stress, therefore, oses, Ceratotherium simum, are associated with high vari- is to pair changes in behavior with changes in physiological ability in the secretion of stress hormones (glucocorticoids) measures, and then examine the precipitating environmen- from the adrenal cortex. Th ey interpreted high variability in tal and/or social events. Measurement of glucocorticoids in fecal corticoids over a one- year collection period as indicat- feces and urine has become the primary means of studying ing an inability of some rhinoceroses to adapt or maintain stress responses in zoo animals and wildlife, because the col- homeostatic levels of adrenal activity. lection method is noninvasive and represents a pooled sample Th ere is also an association of high average glucocorticoid of corticoid output over a period of several hours (Whitten, concentrations with hair loss in polar bears, Ursus maritimus Brockman, and Stavisky ; Möstl and Palme ; Hodges, (Shepherdson, personal communication), and with conspe- Brown, and Heistermann, chap. , this volume). In contrast, cifi c trauma, neoplasia, renal disease, and adrenal cortical sampling blood for corticoid measurement needs to be con- histopathology in clouded leopards, Neofelis nebulosa (Terio ducted more frequently under rigidly controlled conditions and Wielebnowski, personal communication). in order to control for the naturally pulsatile excretion of To address the causes and reduce the deleterious eff ects of corticoids and for circadian rhythms. Th is makes measur- m. elsbeth mcphee and kathy carlstead 305 ing basal levels and changes associated with environmental stead and Seidensticker () interpreted this result to indi- stressors more diffi cult. cate a change in what the bear wanted—mating or foraging Behavior is the animal’s “fi rst line of defense” in response to opportunities. environmental change; it is what animals do to interact with, Two of the most common approaches to determine whether respond to, and control their environment (Mench ). an animal has what it wants are () using environmental mod- Th erefore, behavioral changes must be monitored when as- ifi cations and enrichment to reduce experimentally negative sessing stress in zoo animals. Th e increased occurrence of behaviors such as stereotypy, aggression, and excessive in- repetitive pacing, aggression, excessive sleep or inactivity, or activity, and to increase activity levels and behavioral diver- fear behaviors can be indicative of stress. In a group of so- sity, and () choice tests through which animals may indicate cially housed captive gorillas, Gorilla gorilla gorilla, periods of which behaviors they are most highly motivated to perform. social instability were indicated by elevated glucocorticoids, One explanation for negative behaviors such as stereotypies aggressive displays, and fi ghting (Peel et al. ). Wieleb- is that appetitive motivation to seek something missing in the nowski et al. () found that elevated glucocorticoids in environment causes the animal to channel motivation toward clouded leopards correlated with fur plucking, extensive pac- repetitive locomotion (reviewed in Mason and Latham ; ing, and hiding behavior. A singly housed male orangutan, see Shepherdson, chap. , this volume). In other words, the Pongo spp., had higher glucocorticoid levels on days when the animal cannot fi nd an outlet for its desired behavior. As an keepers recorded his temperament as being “upset” and he example, feeding in the wild constitutes a large portion of refused to shift between enclosures (Carlstead , unpub- some species’ activity budget. Foraging and hunting are pro- lished data). In a zoo- housed giant panda, Ailuropoda mela- cesses that include searching, acquiring (harvesting or cap- noleuca, there was a positive association between glucocor- turing and killing), and consuming food items (Lindburg ticoids, locomotion, and door- directed scratching behavior ). Captive animals, however, rarely have opportunities to and loud noise levels (Owen et al. ). do anything but consume, and oft en that is a compromised Conversely, the frequent occurrence of positive and/or experience, as food is reduced from a complex (e.g. an intact natural behaviors may indicate low levels of stress and, pre- prey item) to an overly simple form (e.g. preprocessed meat). sumably, good welfare. Leopard cats, Felis bengalensis, living In such cases, enrichment in the form of provisioning with in virtually barren cages had chronically elevated glucocor- whole carcasses increases handling time of food and reduces ticoids and high levels of stereotypic pacing that decreased time spent in stereotypic pacing (ibid.; McPhee ). dramatically when they were given the opportunity to hide Choice tests can suggest what the animal “wants” to be or conceal themselves in newly provided complex furnish- doing for pleasure, comfort, or satisfaction and have demon- ings and vegetation. Th ey also increased the amount of time strated that animals usually prefer challenges and engagement spent exploring their cages (Carlstead, Brown, and Seiden- over passive rewards (Mench ). Animals of many species sticker ). Falk (personal communication) reported that, prefer to work for food, such as running a maze or pushing a at one zoo, opening the shift doors for polar bears and giving lever, as opposed to getting food for free. Likewise, they pre- them the choice to go inside or outside greatly reduced ste- fer to explore novel environments and objects. reotypic pacing. Individual white rhinoceroses that keepers Modifi cations to animals’ environments or changes in assess as being most adapted to their captive environment feeding methods frequently reduce negative behaviors and based on how “friendly” they are toward the keeper have increase activity and behavioral diversity (for a review, see lower mean glucocorticoids than conspecifi cs who seem less Swaisgood and Shepherdson  and Shepherdson, chap. relaxed around keepers (Carlstead and Brown ). , this volume). Wiedenmayer () hypothesized that stereotypic digging develops in captive Mongolian gerbils, Meri- ones unguiculatus, because the stimuli that normally cause the DOES THE ANIMAL HAVE WHAT IT WANTS? animal to cease digging were lacking in the captive environ- In zoos, absence of stress and abnormal behaviors are, by ment. He kept young gerbils on a wood- chip substrate with themselves, insuffi cient criteria to ensure animal well- being. access to an artifi cial burrow and found less digging behavior Animals are motivated to perform behaviors (see Shepherd- than in gerbils that were able to dig in a dry, sandy substrate son, chap. , this volume), and animal welfare science seeks to which was incapable of supporting a burrow. identify which behaviors the animal wants/needs to do most In many captive species, stereotypies occur mainly before (e.g. hunting, foraging, swimming). Captive mammals should feeding time, when the animal is motivated to perform food also be active at levels similar to those in the wild (Kagan and acquisition behaviors such as foraging or hunting. Winkel- Veasey, chap. , this volume). Th us, they need to be able to straeter () describes a female ocelot, Leopardus parda- carry out highly motivated behaviors, especially those that lis, that ran in a circular path before feeding. Similarly, Geof- result in a level of behavioral profi ciency that supports the froy’s cats, Felis geoff royi, paced for  to  hours before feeding goals of the program for which they were raised (e.g. rein- time (Carlstead ). Stereotypic behaviors in large felids de- troduction, social living, captive breeding, program animal crease with the provisioning of intact prey items, while food- docile to humans, or exhibit animal displaying normal be- handling time and other consumptive behaviors increase (e.g. havior). Motivations change with the season and reproduc- crouch, stalk, pounce, leap, swipe, bite, hold, eat) (McPhee tive condition; e.g. an American black bear, Ursus americanus, ; Bashaw et al. ). An American black bear paced less had a seasonal pattern of stereotypic pacing where the pac- and explored/foraged more before feeding time when food ing changed temporally and spatially depending on whether was scattered throughout its enclosure (Carlstead, Seiden- it was the mating season or the prewintering season. Carl- sticker, and Baldwin ). Gould and Bres () had some 306 the importance of maintaining natural behaviors in captive mammals success in reducing regurgitation behavior in captive gorillas dus, in Indian zoos used the edge zone of their enclosure for by feeding browse, which increased time spent handling and stereotypic pacing and the “back” zone, farthest from visi- ingesting food. Such studies can be interpreted as meaning tors, for resting. that animals benefi t from the opportunity to “work” for their Of additional interest for future research are the individual food (Markowitz ). diff erences when using operant conditioning to train captive Another fundamental question is whether an animal has animals: learning and performing behaviors could be an in- as much space as it wants or needs in a zoo enclosure. For dication of willingness to work for food rewards or social in- carnivores and other wide-ranging species, home range size teraction with the keeper (see Mellen and MacPhee, chap. predicts the level of pacing in captivity (Clubb and Mason , this volume). Certainly, there are individuals who choose ). With primates, generally the smaller the cage, the more not to be trained, or do so only for their most highly valued some individuals perform stereotypies (Paulk, Dienske, and rewards. Ribbens ; Prescott and Buchanan- Smith ). By increasing the size of the area available to an animal, the be- BEHAVIORAL DEVELOPMENT AND REPRODUCTION havior can sometimes be eliminated or altered (Draper and Bernstein ; Clarke, Juno, and Maple ). Maintaining natural reproductive behaviors in captive-bred Exactly how much space an animal needs is unclear, par- animals is vital to the establishment of self-sustaining cap- ticularly because the critical factor for well-being is oft en the tive populations and maintaining genetic diversity within quality of the space (Berkson, Mason, and Saxon ). Polar those populations. Historically, however, many captive mam- bears have the largest home ranges of all carnivores in the wild mals have reproduced with diffi culty or not at all (Wieleb- and presumably need the most space in zoos—more space, in nowski ). Common problems include inability to court fact, than can be provided by any zoo. Shepherdson’s recent and choose mates, copulate successfully, or rear viable off - multi-institutional study of polar bear stereotypy found that spring, oft en due to a lack of normal species- specifi c inter- enrichment and training is highly negatively correlated with actions with the environment as an animal matures. As with time spent in stereotypy, implying that giving bears some- animal welfare, such developmental problems are observed thing to do continually can be compensation for lack of space at the individual level. (Shepherdson, personal communication). Perkins () and Interactions between the developing organism and its Wilson () found that cage size was not as important for environment start before birth, since the hormonal state of stimulating higher levels of activity in groups of zoo-housed the mother aff ects the uterine environment of the growing great apes (gorillas and orangutans) as was the number and fetus. Th ere are numerous reports of the eff ects of stress ex- type of furnishings. Odberg () compared the behavior of perienced by mothers during pregnancy on the behavior of bank voles, Myodes glareolus, in small, rich environments and their off spring, including increases (Ader and Blefer ) in large, sparse ones, and found less stereotypic jumping in or decreases (Th ompson, Watson, and Charlsworth ) the former. Similarly, spatial confi nement was not a causal in emotionality in a novel environment (open fi eld), altera- factor of stereotypies in Mongolian gerbils (Wiedenmayer tions of exploratory behavior in rats (Archer and Blackman ). Such evidence lends credence to Hediger’s () state- ), and reductions in attack and threat behavior in male ments that the quality of a confi ned animal’s space is more off spring in mice (Harvey and Chevins ). Male off spring important than the quantity. of mother rats stressed daily in the last week of gestation Choice tests are common in animal welfare research of showed reductions in attempted copulations and ejaculation intensive farming practices to determine how much eff ort responses as adults (Ward ). Such studies imply that pre- animals are willing to expend to achieve access to opportu- natal stressors specifi c to a captive environment can cause nities for preferred activities. Dawkins () has used a con- postnatal behavioral changes that reduce reproductive vi- sumer demand model derived from economic theory that ability of off spring. requires animals to work to acquire commodities. For ex- In most mammals, the mother-infant relationship is ample, Mason, Cooper, and Clarebrough () found that critical to the future development of off spring, aff ecting future mink, Mustela vison, expend more energy pressing a weighted defensive responses and reproductive behavior (Cameron door to acquire access to a swimming pool than to gain ac- et al. ). Subtle aspects of the parent-infant or juvenile- cess to toys, novel objects, or alternative nest sites. When peer relationship may aff ect later sexual preferences and com- deprived of pool access they exhibited corticoids elevated to petence, and researchers speak of an extended period of so- a level similar to the corticoid response when they are food cialization occurring during infant and juvenile stages (Aoki, deprived. Th e authors concluded that farmed mink are still Feldman, and Kerr ). A disturbed mother-infant relation- highly motivated to perform aquatic activities despite being ship may deprive the young animal of specifi c stimulation es- bred in captivity without access to pools of water for  gen- sential for the development of normal emotional regulation, erations. social interaction, and complex goal-directed behaviors, in Choice test experiments are not commonly used with zoo particular, maternal and sexual behaviors. Deprivation of animals, because standardizing environments suffi ciently to maternal licking when pups are young has been shown to af- off er  equal choices is diffi cult. However, studies of space fect the timing of sexual behavior patterns in male rats when utilization that divide enclosures into grids can assess ani- grown; intromissions were more slowly paced and the rats mal preferences to some degree, particularly when behavior took longer to ejaculate (Moore ). is also assessed. For example, Mallapur, Qureshi, and Chel- Relationships with peers are also important, especially for lam () found that almost all  leopards, Panthera par- great apes. Maple and Hoff () found that young gorillas m. elsbeth mcphee and kathy carlstead 307 maintained with little or no conspecifi c contact are oft en sex- tive males to display for females and using female reactions ually dysfunctional as adults. Captive female chimpanzees, to guide breeding decisions. Pan troglodytes, are better mothers when they have social ex- Captive mammals, however, are not usually given the op- perience with nonrelated infants or other mothers with in- portunity to assess multiple potential mates and ultimately fants (Hannah and Brotman ). choose an individual suitable to them. Indeed, little is known As an animal matures in captivity, many elements infl u- about how mate preferences develop or are lost in captive ence it that are unique to the captive environment. Close populations. For example, species diff er in whether familiar- contact with humans can produce a range of behavioral char- ity is a good or a bad feature, and in some, the introduction acteristics not found in a wild- reared animal, depending on of an unfamiliar individual as a mate results in high levels of when it occurs during the animal’s development and how aggression. Yamada and Durrant () found that clouded long it is sustained. Th e most signifi cant eff ects of human leopards need to be paired while still sexually immature; in contact on overall behavior likely occur as a result of contact pairs established later, males show extreme aggression toward early in life in lieu of caregiving by the natural mother (i.e. females, oft en resulting in serious or fatal injuries. Female hand rearing) (see also Th ompson, Baker, and Baker, chap. kangaroo rats, Dipodomys heermanni arenae, were less ag- , this volume). In a study of western lowland gorillas, Ryan gressive toward and more responsive to familiar males with et al. () found that mother-reared females had more off - whom they had prior experience (Th ompson ). By con- spring and were more likely to become successful mothers trast, cheetah, Acinonyx jubatus, and white rhinoceroses are than hand- reared females. anecdotally known to be more likely to breed with newly in- Early socialization with humans can aff ect species-specifi c troduced, unfamiliar mates. social skills in both positive and negative ways. Among ungulates with precocial young, fi lial imprinting, in which the BEHAVIORAL DIVERSITY young learn to follow the mother (rather than objects and individuals that do not resemble the mother), occurs within the Animal managers must also be aware of how small, individual fi rst day or two of life (for reviews see Bateson ; Hogan changes aff ect behavioral trait expression at the population and Bolhuis ). Guinea pigs, Cavia porcellus, also exhibit rather than the individual level. Selection in captivity can af- characteristics of fi lial imprinting (Sluckin ; Hess ). fect the expression of behavioral traits in multiple ways; how- Removing a young animal from the mother during this sen- ever, the selective pressures associated with captivity are vastly sitive period may result in following responses being elicited diff erent from those in the wild environments in which spe- by human caregivers, as is commonly seen in sheep and goats, cies have evolved (Hediger ; Price ; Frankham et al. but has also been reported in the American bison, Bison bison, ; Soulé ; Soulé et al. ; Price ; Seidensticker zebra, Equus spp., African buff alo, Syncerus caff er, moufl on, and Forthman ). Captivity can thus impose novel selec- Ovis musimon, and vicuña, Vicugna vicugna (see Hediger tive pressures—either intentionally or inadvertently (Price ). Mellen and MacPhee (chap. , this volume) recom- , ; Endler )—and, over generations, result in mend caution in training young male ungulates, because as changes in important life history and behavioral traits that they mature they tend to show aggression toward humans. aff ect functional relationships between behavioral, morpho- Ideally, captive- born mammals should be socialized with hu- logical, and physiological traits (McDougall et al. ). Un- mans only to the point where they have minimal fear of hu- derstanding and identifying the ultimate mechanisms behind mans (tameness) but still recognize them as heterospecif- behavioral change can be diffi cult, because diff erent selective ics. pressures do not occur in isolation of one another. One trait Many reproductive defi ciencies derive from an inappropri- may experience relaxed selection, while another experiences ate developmental environment, while others occur through directional. Th e overall expression of traits is therefore the lack of opportunities in captivity. In the wild, many mammals result of complicated synergistic eff ects. For the purposes of can choose their mate based on cues ranging from chemical this chapter, we will focus on directional and relaxed selec- odors to complicated courtship displays. Based on such cues, tion. wild individuals tend to choose a mate such that inbreeding Directional selection occurs when the expression of traits is decreased, pathogen resistance is increased, and ultimately, at one end of the distribution is favored (Endler ). In this survival and reproductive success of off spring are maximized case, mean trait expression will shift , but variance around the (Grahn, Langefors, and von Schantz ). Many species have mean will not necessarily change (fi g. .a). For example, evolved mechanisms by which they choose mates that are ge- time spent foraging is a trade-off with predator avoidance netically dissimilar, which reduces the risk of inbreeding for many wild species. More time foraging means more food, (Blouin and Blouin ) and increases the ability of off spring but it also means higher predation risk. On the other hand, to resist disease. House mice, Mus musculus, prefer mates reduced foraging time might decrease probability of preda- that are genetically dissimilar at the major histocompatibil- tion, but the animal will have fewer resources than its bolder ity complex (MHC), a suite of genes responsible for immune counterparts. In the captive environment, that trade-off does function, thus conferring increased immune response and not exist. Some animals that are given foraging opportunities disease resistance in their off spring (Penn and Potts ). may increase the amount of time spent foraging—and as a Grahn, Langefors, and von Schantz () suggest that al- result have healthier off spring and higher reproductive suc- lowing greater mate choice in captive animals might increase cess than individuals who continued to balance foraging and disease resistance in captive populations through increased vigilance. In this case the trait foraging time has been pushed diversity of the MHC. Specifi cally, they suggest allowing cap- in an increasing direction. 308 the importance of maintaining natural behaviors in captive mammals

breeding, a process that may ultimately appear to reduce ge- A netic variance. Artifi cial selection, be it directional or relaxed, can be intentionally or inadvertently imposed. Th e most common form of intentional artifi cial 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 fa- vorable for domestication than others. Easily domesticated species generally live in large, hierarchical social groups in B which the males affi liate with female groups, and mating is promiscuous. Young are precocial and experience a sensitive imprinting period during development. Th ey 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 Fig. 25.1. Directional and relaxed selection. The solid curve represents selective pressures designed to produce a certain outcome, the original distribution of a trait; the dashed curve represents how e.g. increased milk production in dairy cows or long, pointed the distribution changes due to either directional (A) or relaxed (B) snouts in rat-hunting dogs; but many behavioral changes in selection. With directional selection, the mean shifts, but the shape domesticated populations are the indirect consequence of of the distribution does not change; with relaxed selection, the mean selection for other morphological and/or physiological at- remains the same, but the distribution ﬂ attens out, including more values at either extreme. tributes. For example, in Belyaev’s famous selection experiments with silver fox, Vulpes vulpes, animals selected over generations exclusively for tameness also exhibited a shift Relaxed selection can occur when captive conditions from one to  annual estrous cycles (Belyaev and Trut ) permit expression of certain behavioral traits that otherwise as well as phenotypic traits such as fl oppy ears and curly tail would have been selected against in the wild, resulting in an that are typical of domesticated dog species (Trut ). Al- increase in genotypic and phenotypic trait variability (En- though nondomestic captive populations do not undergo dler ; fi g. .b). Consider the time necessary to respond such strong intentional selection, they do experience unin- to a predator. In the wild, animals have limited time to de- tentional selective pressures. For example, temperament in tect a predator and fl ee. In a captive environment, however, captive mammals is likely shaped by directional selection there is typically no predation and individuals can respond (Arnold ; Frankham et al. ; McDougall et al. ). immediately, or never, to perceived threats with no eff ect on In captivity, docile individuals are easier to handle, trans- reproductive success. In this case, relaxed selective pressures port, and medicate than their more aggressive counterparts. in the captive environment result in an increase in variance In a human- controlled environment, docility might translate in response time. into better survival and reproduction, which could lead to In one of the few investigations of population- level behav- unconscious artifi cial selection for docility and tractability ioral processes aff ecting captive mammals, McPhee (a, in mammals—selection that may eventually make captive b, ) tested for directional and relaxed selection in populations divergent from wild populations. On the other captive- bred oldfi eld mice, Peromyscus polionotus subgriseus, hand, Kunzl et al. () compared behavior and physiologi- and found that behavioral and morphological divergence from cal responses of domestic guinea pigs, Cavia aperea f. porcel- the wild population increased with generations in captivity, lus, wild- caught cavies, and captive- bred cavies, Cavia aperea, primarily due to relaxed selection. Trait variance increased sig- bred with no purposeful selection. Th ere were no signifi cant nifi cantly for burrow/refuge use, activity level, response time diff erences between the wild- caught animals and those bred to predators, and skull shape. To our knowledge, this is the in captivity for  generations, suggesting that purposeful only explicit test of these hypotheses in mammals. We recom- selection for specifi c traits may be necessary to produce do- mend more research in this area to identify interspecifi c and mesticated animals. trait-specifi c patterns, as well as linkages between traits. Initially, these increases in behavioral trait variance may CONSERVATION IMPLICATIONS seem counter to the large body of literature that shows that, with generations in captivity, genetic variance decreases. Two Maintaining natural behaviors in captive- bred animals is vital views can potentially resolve this diff erence. First, pheno- to the success of conservation eff orts that rely on those ani- types may be the primary trait on which selection acts (West- mals, such as zoo education and reintroduction of captive- Eberhard ), and minor genetic changes can result in pro- bred animals into their native habitat. found phenotypic changes, which are then selected for (or not). Second, reduced genetic variance resulting from in- VISITOR EXPERIENCE breeding is not natural selection—it is the reduction of genetic variance based on what genes are available. Selection Maintaining good animal welfare is important for not only then acts on the phenotypic expressions that result from in- the individual animal, but also the zoo visitor. Zoos oft en justify the exhibition of exotic species by highlighting the m. elsbeth mcphee and kathy carlstead 309 zoo’s and the species’ educational value. A zoo is likely the to avoid predators, fi nd food, negotiate a complex arboreal only opportunity most people have to see such animals live, environment, and recognize appropriate habitat (Britt, Katz, and most of a visitor’s education while at a zoo comes from and Welch ). In , all known wild black-footed ferrets, watching the exhibited animals (see Routman, Ogden, and Mustela nigripes, were brought into captivity for breeding and Winsten, chap. , this volume). eventual release of off spring. Th e initial releases of captive- Zoo visitors oft en base their evaluation of an animal’s bred ferrets resulted in high mortality due to predation, sug- health and “happiness” on observed behavior (Wolf and Tym- gesting antipredator defi ciencies (Reading et al. ). itz ). In general, visitors tend to be more engaged in front Since many of these problems stem from the fact that the of an exhibit with an active animal (Altman ; Margulis, animals developed and matured in a captive environment, Hoyos, and Anderson ). When that activity is the display such behavioral problems might be eliminated by training of obviously repetitive and abnormal behaviors, however, visi- animals targeted for reintroduction for certain skills before tors perceive animals to be “unhappy” and “bored” (McPhee release. Most work in this area has been done with preda- , unpublished data). tor response behaviors. For juvenile prairie dogs, Cynomys Th rough nature documentaries and other media sources, ludovicianus , prerelease training consisted of exposure to visitors are coming into zoos with more background infor- either a live black- footed ferret, a live prairie rattlesnake, mation than ever before, e.g. knowledge of how animals in Crotalus viridis, or a mounted red-tailed hawk, Buteo ja- the wild behave. Th is knowledge, however, can create false maicensis. All exposures were coupled with the appropriate expectations. Nature programs oft en show carnivores captur- conspecifi c alarm call, but there was no aversive stimulus ing and killing prey. Yet, when visitors see a captive carnivore, associated with the predator presentation. Th is training was it is oft en sleeping (a very natural behavior), and they may suffi cient to enhance survival for at least the fi rst year postre- think it is “bored” and has “nothing to do” (Wolf and Tymitz lease (Shier and Owings ). Similarly, captive- bred Si- ; McPhee , unpublished data). berian polecats, Mustela eversmanni, exposed to predator Exhibit type also infl uences visitor perceptions of natural models (e.g. great horned owl, Bubo virginianus, and bad- behavior. McPhee et al. () surveyed over  Brook- ger, Taxidea taxus) coupled with mildly aversive stimuli, fi eld Zoo (Brookfi eld [Chicago], Illinois) visitors in front of exhibited heightened antipredator responses (Miller et al.  exhibits—an outdoor barren grotto, an outdoor vegetated ). McLean, Lundie-Jenkins, and Jarman () trained grotto, an indoor immersion exhibit, and an outdoor tra- hare-wallabies, Lagorchestes hirsutus, to be cautious in the ditional cage—and found that visitors were more likely to presence of new predators. Prerelease training, especially in perceive animals observed in more naturalistic enclosures as orientation and locomotor behavior, for golden lion tam- behaving naturally and thus being “happy,” compared with arins was not as eff ective as hoped in increasing survival animals in traditional cagelike enclosures. Perceptions of ani- (Kleiman ; Beck ; Beck et al. ). However, pair- mal well-being also strongly aff ected the educational power ing captive-bred individuals with experienced wild-caught of a zoo exhibit. Visitors that observe behaviorally healthy animals did increase the reintroduced animals’ survival rate animals are more likely to walk away with an appreciation (Kleiman ). for that species’ biological signifi cance and need for conser- Prerelease training can also be used to establish hunting vation. Th ese data suggest that, ultimately, an animal’s behav- and foraging behaviors. For example, red wolves, Canis rufus, ior is the most powerful communicator of that individual’s were exposed to carcasses and live prey before release, and health and well-being as well as its natural history and con- swift foxes, Vulpes velox, were given natural foods in the form servation value. 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 REINTRODUCTION that had prerelease conditioning with prey were more effi cient Th ough most zoo animals will spend their entire lives as cap- at locating and killing prey than those without prey experi- tive representatives of their wild counterparts, a very small ence (Vargas and Anderson ). percentage of individuals are targeted for release into their At the population level, understanding how selection has native habitat. Due to changes in important life history and altered the distribution of key behavioral traits within the behavioral traits, however, individuals from an established population may allow reintroduction biologists to compen- captive population are oft en at a disadvantage upon reintro- sate for the observed changes. If the distribution of a trait or duction. Evaluation of reintroduction programs indicates that traits has shift ed signifi cantly, the proportion of individuals many deaths of reintroduced animals are due to behavioral in a population that exhibits natural behaviors will also shift . defi ciencies (Kleiman ; Yalden ; Miller, Hanebury, Mortality will then increase in the release population, because and Vargas ; Biggins et al. ; Britt, Katz, and Welch fewer individuals will exhibit behaviors adapted for the wild ). When golden lion tamarins, Leontopithecus rosalia, environment. If a program’s goal is to release  individuals, were fi rst reintroduced into the coastal rain forests of Brazil, the question becomes how many need to be released such that captive- born animals had defi cient locomotor skills; they  individuals will fall within the natural behavioral range? could not orient themselves spatially; and they were unable To address this question, McPhee and Silverman () de- to recognize natural foods, nonavian predators, and danger- veloped the concept of the release ratio, a calculation that ous nonpredaceous animals (Kleiman et al. ; Stoinski and uses trait variances in release and wild populations to deter- Beck ). Similarly, in Madagascar, reintroduced black- mine the number of release individuals needed such that the and-white ruff ed lemur, Varecia variegata variegata, failed targeted number of individuals exhibits natural behaviors. 310 the importance of maintaining natural behaviors in captive mammals

For example, McPhee’s (a, b, ) behavioral and natural behaviors in captive animals because it is ethically im- morphological measurements of oldfi eld mice showed that perative from the perspective of animal well- being. various traits, such as time to burrow and time in a refuge aft er having been exposed to a predator, exhibited signifi - cant increases in variance. Th us, if a representative sample REFERENCES of the captive population were released into the wild, there Ader, R., and Blefer, M. . Prenatal maternal anxiety and off spring would be more individuals in the tails of trait distributions emotionality in the rat. Psychol. Rep. :– . than would be seen in a wild population, resulting in a higher Altman, J. D. . Animal activity and visitor learning at the zoo. mortality rate than would otherwise be expected. Based on Anthrozoos : – . these data, McPhee and Silverman () calculated release Aoki, K., Feldman, M. W., and Kerr. B. . 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