Zoo Biology 13:413-421 (1994)

Variation in the Parental Care Systems of Mammals and the Impact on Zoo Breeding Programs Anne Baker Burnet Park Zoo, Syracuse, New York

The identity of mammalian caregivers, the types of care each may provide to young, and the developmental, ecological, and social factors that influence the amount and distribution of care are discussed. Care is distinguished from use and abuse in terms of the impact on the survival of young. Some effects of the failure to allow for adequate maternal care are described, and various management strat- egies to promote adequate and appropriate care behaviors are identified. 0 1994 Wiley-Liss, Inc.

Key words: captive management, infant development, maternal care, paternal care, alloparental care

INTRODUCTION

All mammals exhibit some degree of parental care, meaning any behavior that appears likely to increase the fitness of offspring [Clutton-Brock, 19911. Parental care is influenced by a number of evolutionary and ecological factors and has been the subject of a number of monographs and reviews [e.g., Rheingold, 1963; Gubernick and Klopfer, 1981; Elwood, 1983; Taub, 1984; Trivers, 19911. The purpose of this report is to identify those aspects of parental care that are most relevant to the management of mammals in captivity. Management practices that promote good parental care are critical in insuring the success of captive breeding programs. In developing management strategies, it is important to consider not only what parental care behaviors a species exhibits in the wild, but also what selection pressures have shaped those behaviors. This review covers some of the factors that influence parental care behaviors, discusses what impact these may have on management practices at the level of individuals or groups, and concludes with comments about the importance of integrating behavioral considerations into demographic and genetic management plans.

In the broadest sense, parental care includes the preparation of nests and bur-

Received for publication January 10, 1994; revision accepted June 28, 1994.

Address reprint requests to Anne Baker, Burnet Park Zoo, 1 Conservation Place, Syracuse, N Y 13204.

0 1994 Wiley-Liss, Inc.

414 Baker

rows, the care and provisioning of young before and after birth, and the care of offspring after they are nutritionally independent of parents. Among the mammals, maternal care is universal, although sometimes minimal in extent and duration. Male care, including paternal (care by fathers), is found in a number of species, and alloparental (by other conspecifics) care also occurs.

How much care an infant receives and from whom are determined by the interactions among a number of variables: (1 ) the certainty of relatedness between the infant and the caregiver, (2) the benefit-to-cost ratio of the care behavior, and (3) the reproductive value of both the caregiver and the recipient [Hamilton, 19641. Mothers have the highest certainty of relatedness to offspring, and in most mammals they are the primary caregivers [Rheingold, 19631. Paternal care occurs when the male remains with the female, which helps to promote survival of the young, thereby insuring a male’s genetic contribution to the next generation. A male that remains with a female also lowers the risk that a competitor will also breed with that female. This increases the resident male’s certainty of paternity, and therefore the payback to his investment. Certainty of paternity influences not only the extent, but also the types, of care provided. Extensive paternal care is generally tied to certainty of paternity [Werren et al., 19801, and therefore to monogamy, and is found only in a few mammalian families. In multimale, multifemale groups, females may mate with more than one male, and a male’s certainty of paternity for any particular young is low. However, a male has the potential of having fathered some young in the group. In these species, males are unlikely to care directly for an individual young, but instead provide indirect care, such as group defense, that benefits all young in the group [Kleiman and Malcolm, 19811. Many aspects of care involve high energy expenditures and can be costly to caregivers. Both the impact of care on the recipient and the degree of relatedness between caregiver and recipient will determine the benefits of care to the caregiver. In general, mothers will be expected to provide high-cost care, whereas more distant relatives will exhibit low-cost care behaviors.

In some instances, the costs of care may decrease the ability of the caregiver to invest in future offspring, e.g., permitting an offspring to inherit a portion of the parental territory. Reproductive value is a measure of expected future reproductive success [Fisher, 19301. Reproductive value is low at birth, increases as individuals approach sexual maturity, is greatest in the early reproductive years, and decreases thereafter. Individuals that are nearing the end of their lifespan have a low reproduc- tive value, have low expectation of producing many future offspring, and therefore might be expected to invest more heavily in current offspring than would individuals at the beginning of their reproductive years. Similarly, all other things being equal, caregivers might be expected to invest more in offspring that are close to reaching reproductive age than in young juveniles. Degree and certainty of relatedness, cost/ benefit ratio, and reproductive value all interact in an evolutionary sense in deter- mining the distribution of care to young. In turn, these variables are influenced by a multitude of environmental factors. Ultimately the seasonal and spatial distribution of resources and the presence or absence of predators affect the social organization, mating system, and parental care strategy for every species [Alexander, 1974; Alt- mann, 1974; Jarman, 1974; Packer, 1986; Wrangham and Rubenstein, 19861. Re- source availability may determine the costs and benefits of a parental care behavior, such as food sharing, whereas social organization, mating system, and parental care strategy will determine what individuals, other than the mother, are available to

Parental Care and Zoo Breeding 415

provide care and how certain they are of the relatedness to the infant for which they are caring.

At a more proximate level, the developmental state of the infant at birth, the subsequent developmental rate, the willingness of the mother to allow access to an infant, the availability of other infants as the recipients of care, and the behavior of offspring can influence the distribution of both parental and alloparental care. The extent and duration of parental care required by young are strongly influenced by the degree to which young are developed at birth and the rapidity with which young develop physically and socially. Altricial young, i.e., those that are not well devel- oped at birth, are generally born following a shorter gestation period and are a smaller percentage of maternal body weight than are precocial young, which are well devel- oped at birth [Martin and MacLarnon, 19851. Marsupial young fall at the extreme altricial end of the scale. The young of placental mammals fall somewhere along the gradient from altrical to precocial. In general, bats, insectivores, sciuromorph and myomorph rodents, carnivores, and primates produce altricial offspring, whereas hystricomorph rodents, artiodactyls, perissodactyls, and cetaceans produce precocial young.

MATERNAL CARE Maternal care is universal among mammals and can include nest building,

nursing and cleaning young, huddling with young to provide warmth, and transport- ing and protecting young. In some species maternal care extends far beyond weaning, with mothers provisioning young with food, protecting them from conspecifics, and defending them against predators. For animals that live in stable social groups, mothers may play an important role in establishing their offsprings’ social position in the group [Cheney, 19771.

Providing appropriate environments to pregnant females is important in main- taining the pregnancy as well as in producing healthy offspring. Pregnancy and particularly lactation are energetically demanding, and providing adequate nutrition is essential [Sadleir, 1967; Oftedal, 19851. For nest builders or burrowers, appropriate nesting materials or substrate for burrowing should be provided well prior to the expected birth date. In many group-living species, females isolate themselves prior to, during, and immediately following parturition, and the opportunity for isolation should be provided in a captive situation.

Distinct hormonal changes that eventually initiate parturition and lactation occur shortly before birth [Rosenblatt and Siege], 19811. These changes also “prime” the pregnant female to respond to the appearance of young and may result in an increase in female aggression to anything other than young. Almost all mothers will defend their young, and even normally tractable females can become unpredictable when an infant is present. Increasing female aggression may be a signal that birth is imminent, and the mother may need to be separated from conspecifics.

Although the onset of maternal care is governed by endocrine processes, its maintenance depends on sensory stimulation provided by young. The presence of young immediately postpartum appears to be crucial in maintaining maternal respon- siveness to young [Harper, 19811 and providing an environment conducive to main- taining close mother-young contact may be extremely important in insuring good maternal care. Ungulates, e.g. , generally exhibit an immediate postpartum period of intense mother-infant contact, ranging from 40 min in Grants gazelle (Gazella granti)

416 Baker

to up to 200 hr in kudu (Trageluphus strepsiceros). This period is essential for mother-infant recognition and bonding, and only after bonding has occurred will mothers ignore or drive away strange infants [Lent, 19741. Similarly, pinniped moth- ers learn to identify young by vocalizations and scent shortly after birth, and sepa- ration of mothers and infants at this time often results in lack of maternal recognition and care [LeBoeuf and Briggs, 19771. Most terrestrial placental mammal mothers lick the neonate clean [Ewer, 19681. Licking dries the neonate’s coat, which aids in thermoregulation, and often stimulates the onset of breathing, urination, and defeca- tion [Ewer, 19681. Lent [ 19741 suggested that licking increases neuro-excitability in ungulates, promoting more rapid locomotor development of young. Additionally, and importantly, licking provides the mother with gustatory and olfactory input that aids in identification of her infant and often in reducing maternal aggression toward young [Hepper, 1987; Levy and Poindron, 19871. In some species, infants lick their moth- er’s mouth, taking in salivary secretions. This may be important in transferring antibodies [Porter et al., 19801 and/or intestinal flora and fauna that will aid in digestion once weaning has begun.

Nursing begins any time from minutes to hours after birth, depending on the species. In species with multiple births, the female may not suckle the first infant until the remainder have been born, even though the interval may be long.

Because of the high surface area to body weight ratio of many neonates, they do not have sufficient energy to maintain a constant body temperature and require an external source of heat. In most altricial mammals, and in some precocial ones, frequent contact with the mother provides this heat. The prolonged contact necessary for thermoregulation may also function in establishing the bond between mother and infant. Contact with other young, or with older conspecifics, in one nest can serve to conserve body heat when the mother or parents are absent.

Because of the importance of the period immediately following birth for many species, it is extremely vital at this time to provide areas that are some distance from, or out of sight of, public view. In felids and canids, disturbance may result in mothers moving young more frequently than normal [Brady and Ditton, 1979; Leyhausen, 19791, and in canids and ursids, agitated mothers have been known to abandon or kill young [Faust and Scherpner, 1967; Brady and Ditton, 1979; Peel et al., 19791. Primiparous mothers often are especially sensitive to their surroundings immediately following birth, and even the approach of their own infant may startle them, some- times resulting in postponement of mother-young contact and nursing. Although primiparous mothers may be clumsy at first, within a day they usually can care adequately for young.

Although many of the obvious needs of infants can be met in captivity when mothers are absent, there are subtle, sometimes overlooked components of maternal care that play important roles in producing healthy infants, and ultimately healthy adults. There is evidence that mother-infant interactions regulate biochemical and physiological sequences important in growth and development [Butler et al., 1978; Kuhn et al., 1978; Levine, 19821, and experimental studies on rats have shown that early separation from the mothers results in hyperactive young [Hofer, 198 11. For species with long developmental and learning periods, exposure to mothers provides an opportunity for young to learn many of the behaviors that will enable them to survive in their physical and social environments [Hinde and Simpson, 19751.

Parental Care and Zoo Breeding 417

Maternal care can be affected by a number of variables, including the mother’s age, parity, and in social species, dominance rank “ash and Wheeler, 19851. In dolphins and primates, e .g . , primiparous mothers tend to be much more protective of infants (once they have begun to care for them) than are multiparous mothers [Alt- mann, 1980; Amundin, 19861. Primate mothers of high social rank tend to be more permissive with their infants than low-ranking mothers, possibly because high-rank- ing mothers can exert a fair amount of control over how interactions between their infant and other members of the social group will progress [Altmann, 19801.

Regardless of species, age, parity, or rank, all mothers eventually become less tolerant of their infants, and weaning begins. This occurs anywhere from a month postpartum [phocids, Lavigne and Kovacs, 19881 to 4-6 years following birth [great apes, Tuttle, 19861. Weaning may be very abrupt, as is the case with the true seals or occur gradually over a year or more, as in the higher primates. During weaning, mothers may simply refuse to allow infants to nurse, or they may actively punish nursing attempts. Weaning is sometimes met with great resistance on the part of the young, and they may attempt to stay closer to mothers at the onset of weaning than prior to the weaning process.

Weaning is one manifestation of the inevitable conflict between parents and offspring over the extent and duration of parental investment. In mammals, parents are not genetically identical to their offspring, and at some point the costs to the parent of further investment outweigh the benefits, and care should decrease or cease. Because young are more closely related to themselves than they are to siblings, whereas parents are equally related to all offspring, the point at which the cost/benefit ratio shifts is different for patents than for offspring, and offspring should always attempt to garner more investment than parents are willing to provide [Trivers, 1974, 19911. Parent-offspring conflict may arise over weaning, the time at which offspring leave the natal group, access to food and other resources, and where offspring remain in the natal group, over whether offspring breed or assist parents in rearing young [Emlen, 1984; Liberg and von Schanz, 19851. The manager who is sensitive to overt manifestations of parent-offspring conflict often can take steps to mediate its impact. Resolution of conflict may be as simple as separating parents and young for some portion of the day, or for a brief period at the onset of weaning [Smith and Ivins, 19871. Similarly, it is important to take note of dispersal patterns in the wild and to adjust captive management practices accordingly. In some species, such as many of the solitary felids, females drive young away before the birth of the next litter. In captivity, older cubs, when not removed, have been known to maul and kill newborns [Ewer, 19731.

PATERNAL CARE

Although maternal care is universal among mammals, paternal care varies greatly among species. For some monogamous or polyandrous species, such as the marmosets and tamarins, male care begins several hours after birth and in the wild appears to be crucial if young are to survive [Goldizen, 19871. In polygynous species, male care, even if not essential, may improve survivorship. Males may provision either females and/or young, contributing to both the survival of young and to the female’s good condition during lactation. Males may “ babysit,” assuming respon-

418 Baker

sibility for young while females are foraging. In some species, male-young interac- tions play an important role in infant development and socialization [Kleiman and Malcolm, 198 11. Evidence from prairie voles (Microtus ochrogaster) indicates that pups develop more rapidly when the father is present [Wang and Novak, 19941 and the presence of male mice accelerates the onset of female sexual maturity [Vanden- bergh, 1969; Drickamer, 19741. Males in many species take an active role in playing with young, and this assumes added importance in instances when suitable peer playmates are not available, as is often the case in captive situations. For species with an extensive repertory of learned behaviors, adult males provide role models for younger males in developing social behaviors appropriate to mating and reproduction [Kleiman, 1977; Kleiman and Malcolm, 19811.

There are a number of species in which the male has little to do with young in the wild, often because the species is solitary, but for which males and young can be successfully housed together in captive conditions. The potential for paternal care varies across species and often among individuals within a species. Sometimes in these instances, males play with, and are very protective of, young. Why this occurs is not clear, but it may relate to a captive environment that differs greatly from the wild in terms of adequate food resources, or possibly a male’s certainty of paternity. A single male, housed with a female for a long period of time and not subject to the sight, smell, or sound of a conspecific male, may have a lowered propensity for aggression, and therefore may be far more likely to tolerate, and even interact with, young. Instances of male care in captivity have been reported for a number of species in which the male is solitary and therefore has no opportunity to exhibit paternal care in the wild [e.g., felids, Leyhausen, 1979; orangutans, Tuttle, 19861.

Conversely, for species in which males and females normally remain together and fathers care for young, the stresses associated with captivity sometimes can result in a breakdown of normal paternal behaviors. Providing adequate space, visual bar- riers, and multiple den or nest sites may decrease stress substantially, thereby creating an environment conducive to paternal tolerance and/or care of young [Aquilina and Beyer, 1979; Brady and Ditton, 19791. Age and experience of a male, group size, and the presence of maturing subadult males who might destabilize the group are addi- tional factors that can influence male care [Eisenberg, 19811.

Infanticide has been documented in the wild in lions [Bertram, 19761 and several species of primates [Goodall, 1977; Hrdy, 1977; Struhsaker, 1977; Rudran, 19791 and often occurs when an intruder male ousts a resident male. Infanticide may function to bring females into estrous more quickly than if they reared their infants and/or to remove potential competitors to infants sired by the incoming male [Hrdy, 19771. Especially for species in which infanticide is known to occur in the wild, care should be taken when introducing new males to groups with infants. If at all possible, new males should not be introduced until infants have outgrown natal coats and are semiindependent of the mother.

ALLOPARENTAL CARE

Alloparental care ranges from simple, indirect care behaviors such as defense and territory maintenance, to the communal rearing of young by lactating females seen in some bats [McCracken, 19841, rodents [Hoogland, 198 1 J , canids [Malcolm and Marten, 19821, and African lions [Schaller, 19721. A number of variables can

Parental Care and Zoo Breeding 419

influence the extent of alloparental care. It will depend in part on opportunity, which in turn depends on the restrictiveness or permissiveness of the mother. Age, sex, and rank of the potential caregiver also may influence the mother’s willingness to allow that caregiver access to her infant.

Not everything that initially appears to be alloparental care truly benefits in- fants. Some interactions between infants and nonparental group members may fall under the category of use, or in some instances, abuse. Adult male Barbary macaques (Macaca sylvanus) carry infants during dyadic agonistic encounters [Deag and Crook, 19711. It is thought that infants serve to buffer the carrying male from attacks by the other male. Infants are rarely harmed in these interactions, but neither are they receiving care from the adult males. Similarly, inexperienced females may use infants to “practice” mothering. Although such “practice” may not actually harm infants, it does not qualify as care, but falls instead under the category of “use.” In some instances infants may be “kidnapped,” and evidence from macaques [Silk, 19801 suggests that this practice is a form of competitive interference that negatively affects infants by preventing them from nursing. In the confines of captive enclosures, low-ranking mothers particularly may find it difficult to avoid interference from other group members. If interference becomes too frequent, it can result in harm to the infant, and steps to mediate interactions may be required.

POPULATION MANAGEMENT CONCERNS Demographic and genetic recommendations generated by SSP masterplans

sometimes conflict with good behavioral management. When this happens, popula- tion managers and managers of individual animals must work together to resolve the problems. For example, as population managers attempt to decrease the numbers of individuals required to maintain healthy captive populations, they often recommend increasing generation time by increasing interbirth intervals. This creates problems for species, such as the callitrichids, in which learning plays an important role in the establishment of parental care behaviors. Youngsters that have had the opportunity to care for younger siblings are better parents than youngsters lacking that experience [Hoage, 1977; Snowdon et al., 19851. Long interbirth intervals mean that there will be no younger siblings around for older siblings to care for prior to reaching sexual maturity and being expelled from the natal group, and hence no opportunity to practice parental care skills. Possible solutions to the problem might include increas- ing generation time by delaying timing of first reproduction, or a program that phases breeding and moves younger siblings out of the group along with older ones as the older ones are paired, thereby allowing the younger siblings to gain experience with their nieces and nephews rather than with brothers and sisters. There are often mul- tiple solutions to a problem, but none can be implemented if the behavior of the species is not taken into account in developing a course of action for implementing the management plan.

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