Early social experience and subsequent sexual behaviour
(in other species)
In general, early social deprivation negatively influences nonhuman primate sexual behaviour, but more strongly in males than females
(Mason et al., 1968; Reisen, 1971; Sackett, 1974). Male and female macaques (Macaca spp.) raised without mothers experience a variety of deficiencies in sexual behaviour, both in form (e.g. improperly oriented mounting) and sequence (e.g. male genital examination is not followed by male positioning or female presentation) (Mason 1960; Harlow, 1969; Testa & Mack, 1977). The mechanism by which this occurs seems to be through insufficient coordination and communication rather than an inability to perform any individual behavioural component (Capitanio, 1986). In the chimpanzee (Pan spp.), both male and female offspring that are removed from the mother and then reared by humans are less proficient at copulating (Davenport & Rogers, 1970; Reisen, 1971). However, it appears that the level of nursery management can influence this outcome. With more intensive nursery practices involving the presence of peer youngsters and extensive human care, these chimpanzees can normally copulate and reproduce, although they still express less frequent sexual behaviours than mother-reared counterparts (Bloomsmith & Baker, 2001).
Rearing domestic carnivores in socially deprived conditions also results in sexual behaviour deficiencies. Female domestic cats hand-reared and isolated from conspecifics show fewer courtship, amicable and copulatory behaviours than mother-nurtured females or those reared with siblings (Mellen, 1989, 1992). Additionally, female kittens that grow up with siblings are more sexually competent than females reared in isolation but less competent than mother-reared counterparts. Male dogs developed in isolation have sexual behaviour deficiencies unlike males raised in groups or with limited peer contact (Beach, 1968).
There are well-recognised breeding challenges in a host of wild carnivores maintained in captivity, including the cheetah (Caro, 1993; Wielebnowski, 1999), clouded leopard (Yamada & Durrant, 1989), small-sized felids in the genus Felis (Mellen, 1991) and the maned wolf (Rodden et al., 1996). Although there has been little experimental research in these or other wild carnivores, preliminary findings to date have been unable to link early social deprivation to current reproductive problems (Mellen, 1991; Wielebnowski, 1999).
Early social experience and subsequent sexual behaviour
(in the giant panda)
For the giant panda, a primary behavioural challenge is that many females do not display behaviours normally associated with oestrus
(Zheng et al, 1997). This is especially important given that a female has only one period of receptivity per year (one three-day oestrus) to copulate for producing offspring. In one ex situ population survey, 21 of the 43 breeding-age females (6 to 20 years of age) had not produced any surviving offspring (J. Ballou, pers. comm.). Nine of these were wild-born and, thus, critical recruits to the breeding programme as founders (Zheng et al, 1997; see also Chapter 21). Nonbreeding males either lack sexual interest or show aggression toward oestrual females (Zheng et al., 1997; see also Chapter 3).
As of 1997, fewer captive males (29.3%; n = 12) than females (45.7%; n = 21) had produced offspring (Lindburg et al, 1997; Zheng et al., 1997). As of 2003, the situation had improved with 50% (17 of 34) of males and 51.2% (22 of 43) of females producing surviving young. However, a more recent examination revealed that, of 56 adults (19 males, 37 females), 36.8% of males had copulated versus 48.6% of females (S. Sun, pers. comm.). Therefore, a lower proportion of males are reproductively successful, largely due to an inability to exhibit successful sexual behaviours. Lindburg et al. (1997) examined a variety of factors potentially influencing reproductive success of male pandas housed in Chinese breeding centres and zoos. Although the importance of early rearing history per se was not examined, these investigators stated that ''early rearing deficiencies could be one of several factors contributing to mating dysfunction in male adults''.
The lower reproductive success of captive males compared to females indicates that early removal from the mother may impact young male pandas more than young females, as has been found for primates. In nature, male and female giant pandas play very different social roles. Males have larger home ranges, spend more time travelling, compete and fight for access to oestrual females and do not care for young (Schaller et al, 1985). By contrast, females are solely responsible for offspring rearing, thereby concentrating their activities over a more restricted habitat range that has the required resources to contribute to successful cub rearing (Schaller et al., 1985).
If there are fundamental differences in the social requirements for young males to develop the necessary skills to reproduce, then one would expect to find within species sex differences in early behavioural development. In fact, young male pandas spend significantly more time play-fighting with their mothers than do young females (Snyder et al., 2003). We have not found sex differences for other general categories of behaviour, including locomotion or self-motion play (i.e. a variety of
nondirected body movements, including rolling, headstand and somersaulting that do not result in travel from one point to another). Sexual differentiation of play is most common in juveniles of species in which males and females have different adult roles. Certainly, this is the case for giant pandas. Thus, the play-fighting of young male pandas may prepare them for aggressive encounters with rivals in adulthood (Fig. 14.1).
Although giant panda males are reproductively mature at five to six years of age (Schaller et al., 1985), some captive-held males do not begin breeding until much later. For example, one male (SB number 342) at the Chengdu Research Base did not copulate until 14 years of age (Snyder, unpublished data) despite being given access to at least one oestrous female each year from the time he was four to seven years of age. He was aggressive during some of these early introductions, and, because he mildly injured two females, was not given the opportunity to breed again until age 14, when he was suddenly successful. Another male (SB 287) at Chengdu Zoo was placed with prime age females at seven and eight years of age but no breeding occurred. When given the opportunity again at age 13, he mated successfully. Both SB 342 and 287 were captured from the wild at less than one year old and, thus, may have had a few more months of mother-rearing than typical captive-born counterparts. In retrospect, both may have been capable of breeding at earlier ages than when mating actually occurred (at 13 and 14 years, respectively). However, because these males were labelled as hyper-aggressive or nonbreeders, there were limited (or no) further opportunities for mating until later years. Therefore, we believe that caution should be used in qualifying animals with labels such as 'non-breeder'. Males (even if not successful at the first attempt) need to learn breeding behaviours, and this is possible only through regular exposure to oestrual females. We recommend allowing a male to interact with females though a barrier, which provides olfactory, visual and limited tactile contact. The male's and female's behaviour can be safely assessed and used to decide if free access should be given. If possible, a male should be given this type of exposure to several different females in each breeding season, because some pairs are more compatible than others (Snyder et al., 2004). This strategy has been used successfully at the Chengdu Research Base since 2001 and has been facilitated by the construction of a new facility with enclosures specifically designed for these types of breeding introduction.
Some captive females also do not mate until well into their adult years. For example, two females (SB 297 and 314) from the Chengdu institutions copulated for the first time at 12 years of age. These females were introduced to an experienced male every year during their oes-trous cycles for six to seven years before finally mating. Although both displayed obvious behavioural changes associated with oestrus and were characterised by the Chengdu staff as having strong oestrus, each failed to hold a lordotic posture when the male mounted. Rather, each female would sit, walk away or put her tail down during the copulatory attempt. Interestingly, these observations were similar to Mellen's (1992) findings for the isolate-reared female domestic cat which can behave in a similar manner. Also, SB 297 and 314, which were slow to acquire copulatory behavioural skills, were captive born and reared similarly to other Chengdu-born females that copulated at four to six years old. Therefore, we conclude that early rearing history is not the only variable predictive of later sexual behaviour.
Applying knowledge about breeding interactions in wild giant pandas may offer insight into the problem of delayed breeding success in captive individuals. Wild male giant pandas congregate around a given oestrous female and fight for breeding access, and a female sometimes mates with more than one male from such assemblages (Schaller et al., 1985). It has been hypothesised that the largest, most experienced male dominates these interactions, breeds with a female early in oestrus (ensuring that his sperm are in the oviduct at the time of ovulation) and then moves on in search of other females (Schaller et al., 1985). The female continues to be receptive for a short time thereafter, mating with other, possibly younger males who were a part of the original congregation. This system is probably one way young males acquire the motor skills necessary for successful copulation. This process also has the advantage of allowing a young male the opportunity to mate with an experienced partner, which might assist with learning correct positioning and sequencing of behaviours. Young males in a particular area might encounter several receptive females each year offering multiple opportunities to practice copulation. The female also benefits from the multiple matings by ensuring the presence of plenty of viable sperm at the time of her ovulation.
Applying this multi-male mating strategy in captivity is not as simple as it might seem, largely because of the risk of injury. Unlike in nature, where there is plenty of room to escape in the presence of behavioural incompatibility, captive situations (by definition) do not provide the same opportunities to flee. Thus, injuries can and do occur during breeding encounters. Nonetheless, it is possible to give a young, inexperienced male access to a receptive female, especially after she has mated with a more experienced male. This opportunity has not been a routine part of captive giant panda management in China but should be tested and evaluated. If successful in enabling more males to copulate at a younger age, then it may be necessary to rethink the current model, especially for smaller institutions and those outside China that usually hold only a single pair. Perhaps it makes more sense to hold a minimum of three or four individuals, where there is the opportunity for a young male to have frequent encounters with an older, experienced female. Therefore, a female is maintained not only as a breeder (with a compatible, older adult), but also as a mentor for an inexperienced, young male.
Early social experience and subsequent maternal behaviour (in other species)
The early social environment can influence adult maternal behaviour. Experimental and anecdotal reports provide a consistent picture of infant neglect, abuse and infanticide by nonhuman primates that lacked normal social experiences (Ruppenthal et al, 1976; Capitanio,
1986; Beck & Power, 1988) with rearing in social isolation causing the most severe later maternal deficits. Chimpanzee mothers raised by humans in a nursery are less likely to care for their own infants than mother-raised counterparts (Brent et al, 1996; Bloomsmith et al., 2003). For example, 65% of nursery/peer-reared chimpanzee females were incompetent primiparous mothers (Bloomsmith et al, 2003). The result is a cycle of parental incompetency that is passed from one generation of nursery-reared primates to another (Maple, 1980). The relatively severe consequences for apes may be the result of motor immaturity at birth, a prolonged period of infancy and the long duration of dependency on the dam.
Depending upon litter size, solitary carnivores spend most of their early development associated with the mother alone with or without siblings (Ewer, 1973). Carnivore offspring are invariably altricial, that is highly dependent on parental care (although no other carnivore is so much so as the giant panda). The period of dependence of many large carnivores is long (Ewer, 1973), and the age of independence is greatest in the ursids (Ewer, 1973; Gittleman, 1986).
Although zoo professionals widely believe that mother-rearing increases the likelihood of producing individuals with good parenting skills, very little experimental or archival data are available for species other than primates and rodents (Baker et al., 1996). There are many accounts of captive, wild carnivore mothers abandoning or cannibalising their young. Most of these reports cite disturbance by humans and noisy environments as possible proximate causes (Flint, 1975; Vogt et al., 1980; Aquilina, 1981). Experimental evidence indicates that carnivores reared in socially deprived settings also exhibit later deficiencies in maternal behaviour. Two female domestic kittens removed from their mothers at seven weeks of age and subsequently reared in isolation cannibalised their first litters (Baerends-van Roon & Baerends, 1979). The maternal behaviour of one of these females improved with experience (she successfully raised later litters), but the other continued to cannibalise litters. Mellen (1989) attempted to examine the effects of early rearing on maternal behaviour by raising domestic kittens in three conditions: mother-reared with sibling; hand-reared with sibling; and hand-reared in isolation. Little could be deduced about maternal behaviour because sexual behaviour was so detrimentally affected by hand-rearing - only one female in each of the hand-reared groups ever conceived. Both of these females were adequate mothers and successfully raised their litters to independence.
Early social experience and subsequent maternal behaviour (in the giant panda)
Giant pandas give birth to the most altricial offspring of all placental mammals (Zhu et al, 2001). According to Grand (1992), more than 99% of giant panda brain and body growth occurs postnatally. Thus, giant pandas have greater motor immaturity and prolonged infancy and dependency on the mother than any other carnivore. Most solitary species give birth to multiple young, and littermates play an important role in sociosexual development. Such development in the giant panda is unusual because the female normally rears only one offspring. Thus, in the wild, a cub's first several months of development are spent entirely in the company of the mother, whose role in offspring socialisation may be especially critical. Giant panda cubs have a relatively long period of maternal dependency similar to that of other bear species whose cubs are not fully weaned until two or more years of age (Gittleman, 1986). Therefore, we might expect giant panda maternal behaviour to be strongly impacted by early rearing deficits.
In the past at the Chengdu institutions, females were raised by their dams until four to six months of age, after which they were separated and placed with at least one peer until the age of three to four years. After this time, each female was typically housed with one to three other adult females. Six of the nine females examined were competent first time mothers, naturally breeding at 4 to 12 years. This high proportion of success probably indicates that mother-rearing for the first few months followed by peer-rearing may be sufficient to develop adequate mothering skills in this species (X. M. Huang & S. Zhong, pers. comm.). There also is evidence that females with less than four months of mother-rearing may not become competent mothers. One female (SB 425) was hand-raised alone for her first year of life, after which she was placed with peers. Although she has never mated, she has given birth three times via AI and rejected all three of her cubs. Another female (SB 314), with only one month of mother-rearing, displayed inappropriate maternal care with her first three births (all twins). She held her cubs too tightly (two cubs died from injuries that may have been the result of squeezing by the mother), did not hold them near her nipples and licked her own rather than the cubs' fur (X. M. Huang & S. Zhong, pers. comm.). However, it is worth noting that another female (SB 401), raised similarly to the maternally competent females, also rejected her first cub. Therefore, more data are needed to determine whether females hand-reared from a very early age have a higher incidence of cub rejection than counterparts that were removed from their mothers at a few months of age and subsequently lived with peers. A high priority is determining the time-frame or critical period after which removal from the mother does not impair subsequent maternal behaviour.
It is important to note that female giant pandas that initially reject cubs or exhibit other inadequate mothering behaviours can later acquire these skills. This was demonstrated by Zhang and colleagues (2000) at the China Conservation and Research Centre for the Giant Panda (Wolong Nature Reserve). A primiparous female (SB 446) was provided with controlled periodic access to a cub that she had rejected at birth. These investigators documented the dam mastering specific care-giving behaviours until the cub could be fully returned to its mother at 73 days of age. Corroborating anecdotal evidence is also available from the Chengdu institutions where females are normally categorised on a 1 to 10 scale for mothering skills (10 being the best rating). Female (SB 314) was rated as a 4 for mothering skills for her first three births, and her cubs died or were removed by six days of age for hand-rearing. However, the staff continued to give her the opportunity to raise subsequent cubs, and by her fourth birth she rated a 7 on the 'mothering meter' and cared for her cub for five months according to standard management in Chengdu.
Female giant pandas exhibit tremendous flexibility in their maternal behaviour and associated tolerances, including extending their mothering behaviour to multiple young not their own (see below). The ability to cross-foster increases infant survivorship and the quality of life for cubs under an intensive management system. It also probably provides a unique socialisation opportunity for cubs while allowing some females to return more quickly to the breeding population. For example, it is well known that some dams will tolerate offspring swapping - the periodic switching of infants from the dam to the nursery thereby allowing a given female to nurse multiple offspring.
In theory, genetically valuable females could be reserved for offspring production but not cub rearing - with these females then allowed to recycle and rebreed on an annual basis. Schaller and colleagues (1985) speculated about the phenomenon of twinning in the giant panda. They suggested that wild female pandas abandon one twin cub because of energy constraints, as well as the high level of care-giving required by two extremely altricial neonates (Zhu et al, 2001). A captive female's willingness to care for multiple cubs simultaneously may indicate that she retains the behavioural flexibility to raise a litter and/or the realisation that energy requirements for raising more than one offspring are being readily met in the captive environment.
The first successful cross-fostering of a giant panda cub from one mother to another at the Chengdu institutions occurred in 1990. This strategy is now practised routinely here and elsewhere, most often for a rejected cub or often when twins are produced. Mothers accepting cross-fostered cubs do not hesitate to accept another female's cub, and there is no indication that they distinguished the unrelated cubs from their own. Cross-fostering has been successful with cubs varying in age from a few hours to several months. In Chinese institutions, giant panda females typically give birth within a few weeks of each other. Thus, all the cubs born at the Chengdu institutions in a particular year are similar in age and size, which may contribute to the likelihood that a cub from one mother will be accepted by another. Four dams (SB 278, 297, 362 and 314) at the Chengdu Research Base have been successful foster mothers, including nursing and playing with all cubs (Fig. 14.2). When cubs are less than four months old, a mother is usually given only one cub at a time. However, when cubs are more than four months of age (when they are walking, urinating and defecating on their own), a mother may care for two or more cubs concurrently. Amazingly, some dams have cared for as many as four cubs simultaneously. No attempt has yet been made in the Chengdu institutions to introduce a cub to a nonlactating female without a cub of her own.
Early social experience and subsequent aggressive behaviour
(in other species)
Many nonhuman primates raised in isolation from conspecifics (especially from their mothers) are hyperaggressive when placed in social situations (Mason, 1960; Baker & Aureli, 2000), with males being more aggressive than females (Meder, 1989). It may be that the nursery/peer-rearing experience (which offers little or no understanding about the consequences of inappropriate hostility) produces animals that display aggression at abnormally high rates. Nonhuman primates with histories
of social isolation also can be hyperfearful, sometimes engaging in almost no positive social behaviour (Mitchell et al, 1966). While there is some variation in onset and degree of hyperaggression and fearful-ness (Capitanio, 1986), it is clear that early social deprivation disrupts the incidence of agonistic interactions.
Similar findings occur in the domestic cat. Kuo (1960) found that kittens raised with rats and in isolation from conspecifics were hyperaggressive toward conspecifics later in life. Age of separation from the mother affects the development of antagonistic behaviour. Seitz (1959) reared kittens in isolation after removing them from their mothers and littermates at 2, 6 or 12 months of age. Individuals isolated from 2 weeks of life were most aggressive and fearful toward conspecifics and humans. Mellen (1989,1992) found that female kittens reared with their mother and one sibling exhibited the least aggression toward males during their eventual oestrus. She also reported that cats reared alone by humans were excessively hostile toward humans compared to mother-reared counterparts exposed to a sibling. The latter (unlike the former) were calm and friendly. Kittens raised in isolation from one week (Weiss, 1952) or seven weeks (Baerends-van Roon & Baerends, 1979) of age also try to escape when later placed with conspecifics.
For captive wildlife species, hyperaggression has been documented in certain carnivores. The clouded leopard is notoriously difficult to breed in captivity because of intersexual aggression by males, which has resulted in serious injury or death of females at 22 of 44 institutions (Yamada & Durrant, 1989).
Managing aggression in captive giant pandas can be challenging, particularly during breeding introductions involving unfamiliar individuals. Male hyperaggression is a main reason cited for breeding failure in captivity (Zheng et al, 1997; see also Chapter 3). In the wild, aggression may be valuable for competing with other males. Captive males, however, live in isolation because of the potential for injury if contact was allowed. Hyperaggression in captivity may be an expression of a species-typical behaviour with no outlet and, thus, is misdirected toward females. Furthermore, the intensity of the interaction, or perhaps inappropriate responses to interactions that escalate rather than tempering aggression, may be a result of early rearing practices common in managing giant pandas.
Variations in male assertiveness may be driven by seasonal patterns in testosterone (a recently discovered rhythm in this species; see Chapter 8). Giant pandas living in nature are probably familiar with other nearby residents (via chemical communication or even occasional chance meetings or possibly involvement in previous breeding congregations). Captive individuals are often not given much opportunity to become familiar with each other prior to breeding introductions. Thus, it is possible that some males do not recognise a female that is in oestrus when introduced for breeding, and first reactions are aggressive rather than sexual.
Because the less aggressive males are easier to manage in breeding introductions, these giant pandas are used most often for mating to the exclusion of more assertive individuals. The former's genes then become common in the population, whereas the latter males become more genetically valuable (see Chapter 21). Therefore, the current management regimen selects against aggression, a trait that is probably essential to survival and the spreading of one's genes in nature. This may not be an immediate problem for the ex situ population, given continued improvements in AI. However, if the reintroduction of captive individuals to the wild is ever to be successful, behaviourally competent individuals with the social skills necessary to interact appropriately with wild conspecifics will be essential.
Approaches have been developed for other species (Burks et al., 2001) which allow aggression to be managed or circumvented to permit breeding and to minimise injury. This usually involves a step-wise process that controls exposure between adults to allow developing familiarity before the breeding introduction. Individuals first have visual and olfactory contact, then limited tactile contact and finally full access in a controlled setting. This strategy for resocialising individuals with hyperaggressive histories warrants attention for the giant panda, especially as a means of recruiting genetically, underrepresented males into the population.
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