Fifty years of chimpanzee demography at Taronga Park Zoo

There has been a captive Pan troglodytes colony at Taronga Park Zoo in Sydney, Australia, since the mid-1930s. Demographic data on these animals were first analyzed in 1986; however, further information collected for 15 years since then is now available. The reproductive histories of 33 females in the colony have been recorded, and these data form the largest collection of captive chimpanzee data from a setting that has involved natural breeding conditions since the mid-1960s. These data were analyzed in conjunction with data from wild populations to establish the degree of variability present within chimpanzee reproductive parameters, and to identify which distinctive life history characteristics persist in well-provisioned, natural-fertility populations. The age at first birth for the chimpanzee females is 9.8 yr on average (n=16), which is 1-4.8 yr earlier than the average for wild populations. In line with this accelerated reproduction, birth intervals are also significantly shorter than those in noncaptive chimpanzee populations. The median birth interval for all surviving infants (based on a Kaplan-Meier survival analysis) is 49 months (n=43) compared to 62+ months for wild groups. At the same time, infant mortality remains high. The data confirm distinctive features of the life history of common chimpanzees, including later maturation, long birth intervals, a relatively invariant fertility schedule, and high juvenile mortality. However, aspects of both fertility and mortality are significantly related to social circumstances, indicating that in common chimpanzees, as in humans, life history characters may represent ecological and social adaptations rather than species-fixed characteristics.     

BEHAVIORAL SIGNIFICANCE OF UNDERWATER VOCALIZATIONS OF CAPTIVE LEOPARD SEALS, HYDURGA LEPTONYX

Two groups of underwater vocalizations were identified in a three-year study of two captive leopard seals, Hydurga leptonyx (one female and one male at Taronga Zoo, Sydney). This was supplemented by recordings over three months from a male at Marineland, New Zealand. The sexual state of the seals at Taronga was deduced from serum hormonal concentrations: the female was considered to be in estrus at specific times during the breeding season. The seal at Marineland, New Zealand was assumed to be sexually mature on the basis of size and age. Of 12 different underwater sound types recorded, six were produced by the seals at Taronga Zoo during agonistic interactions (local calls) and were heard through most of the year. The other six sound types were produced by lone seals. These broadcast calls were produced by the female only when sexually receptive, and by the mature male during December and January, months believed to be the breeding season of wild leopard seals. We propose that underwater acoustic behavior is important in the mating system of this species, and that broadcast calls are used by mature females to advertise their sexual receptivity, and possibly by mature males in search of mates.     

Determinants of breast-feeding and post-partum amenorrhoea in Orissa

A life table analysis is made of the duration of breast-feeding and post-partum amenorrhoea in Orissa, India, taking one variable at a time using data from a baseline survey of fertility and mortality (BSFM) conducted on the lines of the World Fertility Survey. Then a multivariate (proportional hazard) analysis showed that socioeconomic factors including residence, caste status and education influence the breast-feeding and post-partum amenorrhoea periods. There was no effect of maternal age on the length of breast-feeding, but mean length of post-partum amenorrhoea varied with age. The durations of breast-feeding and post-partum amenorrhoea are strongly related.     

Measurement of post-partum amenorrhoea in Bangladesh.

Reported information on the duration of post-partum amenorrhoea usually shows considerable number preference, particularly at 6-monthly intervals. This paper presents a technique for smoothing such amenorrhoea data using a modified exponential curve. An attempt has also been made to estimate the average number of months a mother is expected to remain amenorrhoeic.     

Health of adult free-living cheetahs

Health of free-living adult cheetahs was assessed using haematological and biochemical measurements of condition. Results showed that cheetahs of both sexes varied on several of these measures, demonstrating that their genetic monomorphism does not result in individuals being of equivalent health. Differences in condition appeared to be somewhat associated with sex, age and whether males were territorial. Compared to two different groups of captive cheetahs, free-living cheetahs were monocytotic, and free-living females were macrocytic. Limited data from captive animals showed they ate more than their free-living counterparts, possibly reflecting the elevated blood glucose levels of captive cheetahs.     

Mass transfer from mothers to pups and mass recovery by mothers during the post-breeding foraging period in southern elephant seals (Mirounga leonina) at King George Island

Mass transfer from mother to pup during the lactation period, and mass recovery for the same females during the foraging period were measured in the southern elephant seal at King George Island, Antarctica. During the 19.2 ± 0.9-day lactation period measured (which represented 87% of the entire nursing), females lost a mean mass of 10.56 ± 1.76 kg/day (n = 27), while their pups gained a mean mass of 5.27 ± 1.1 kg/day. There was a correlation between daily body weight gain in pups and daily weight loss by their mothers. Pup weaning mass was positively related to maternal post-partum mass. Serial samples showed that weight losses by females and gains by their pups were not linear over lactation, but showed lower values at the beginning and at the end of lactation. During the 60.5 ± 6.2-day foraging phase between the end of lactation and molt, females gained 2.21 ± 0.65 kg/day (n = 12), or 54% of the mass lost during nursing. Growth rates reported here are higher than those reported in other breeding sites. However, the ratio of body mass loss by females to gain by their pups was similar, suggesting that higher growth rates and greater weaning mass at South Shetland are due to a higher mean weight of females on arrival at this breeding site. The foraging period was shorter and the mass gained greater than those measured at South Georgia; this could be related to relatively shorter distances to foraging areas. Received: 20 September 1996 / Accepted: 28 April 1997     

Captive breeding, paternity determination, and genetic variation in chimpanzees (Pan troglodytes) in the Australasian region

DNA “fingerprinting” using polymorphic (CA)-repeat microsatellite markers was used to quantify the level of genetic variation present in chimpanzees (Pan troglodytes) in the Australasian region. These markers were also used to determine the paternity of chimpanzees born at Taronga Zoo over a 20-year period. The results suggested that the dominant male in the colony was responsible for siring most, but not all, of the offspring. Where the dominant male was excluded from paternity, the sire was identifiable if all candidate males were available for typing. This enabled us to prove the captive origin of offspring born in the colony during this period. Thus, microsatellite analysis was a useful tool for assignment of familial relationships and improving genetic management of breeding colonies.     

Seasonal changes in the blood composition of captive and free-living White-crowned Sparrows

Summary Seasonal changes in several blood components (cholesterol, phospholipid phosphorus, glyceride glycerol, free fatty acids, and calcium), hematocrit, and body mass were studied in captive and free-living groups of White-crowned Sparrows (Zonotrichia leucophrys gambelii) over a 2-year period. Cholesterol, phospholipid phosphorus, and glyceride glycerol levels were correlated with body mass and all of them changed in parallel during the year (Table 2 and Figs. 1–3). These lipids were elevated during premigratory and migratory periods, minimal during the summer breeding period, and reduced during periods of body molt. Concentrations of them were consistently higher in captive birds than in free-living ones. Free fatty acid levels were highly variable and not correlated with levels of other blood lipids or with body mass (Fig. 4). However, they too increased during premigratory periods. On the other hand, they were consistently higher in free-living sparrows than in captives. Plasma calcium was relatively constant at 3–5 mEq/l between July and the following March (Fig. 5). It increased during the spring, but earlier than preparations for migration by 2–3 weeks. It was also elevated in egg-laying females. The hematocrit rose during the vernal migratory period, but not during the autumnal one; was minimal in breeding birds; and declined during periods of body molt (Fig. 6). Calcium and hematocrit levels were similar in captive and free-living birds. It appears that captive populations of White-crowned Sparrows generally provide relibale information concerning changes in blood composition that are taking place concurrently in the field.This investigation was done to satisfy partially the requirements for the Ph.D. degree at Washington State University by deGraw and Kern. The project was supported by an NIH Training Grant (GM01276) from the National Institute of General Medical Sciences     

Plasticity of Alarm-call Response Development in Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Plasticity in the alarm-call responses of Belding's ground squirrels ( Spermophilus beldingi ) may function to prepare young to respond appropriately to calls according to the predator environment and habitat in which the young develop. To examine the extent to which antipredator responses are sensitive to early rearing environments, we studied the development of behavioural responses to playbacks of alarm calls and non-alarm calls in free-living juveniles and captive juveniles housed in large outdoor enclosures. Compared with same-aged, free-living juveniles, captive juveniles were more likely to show an observable response to playbacks, exhibited more exaggerated initial responses (e.g. enter a burrow vs. freeze), and remained alert longer following playbacks. The influence of rearing history on antipredator responses was limited to responses to auditory stimuli, as the two groups of juveniles reacted similarly to fast-moving visual stimuli. The responses of free-living juveniles appeared to be more discriminating than responses of captive juveniles, particularly following playbacks of calls associated with less immediate threats.
The responses of captive and free-living mothers were similar, indicating a developmental component to the juvenile response differences observed here. Free-living juveniles developed a discrimination among alarm and non-alarm calls sooner than captive young. Response differences were evident within 1 wk of first emergence from natal burrows and persisted at least 4 wk, at around the age of natal dispersal. This suggests that early rearing history has an enduring effect on response repertoires, which may be adaptive if animals continue to inhabit the predator environment in which they developed.     

Behavioral solutions to breeding cheetahs in captivity: Insights from the wild

Knowledge of cheetahs' behavior is increasingly seen as the key to solving the mystery of cheetahs' poor breeding performance in captivity. In the absence of zoos' maintaining systematic records of individuals' behavior during introductions, behavior of free-living animals can be informative. In the wild, most female cheetahs probably mate with males living in small groups or coalitions; thus, zoos may benefit from replicating these social conditions, provided injuries can be minimized. Relations between free-living coalition members are amicable, and escalated aggression was never witnessed during 4 years of observation. Some antagonism was seen in newly formed trios, although this had disappeared in longer established coalitions. Minor aggression occurred over carcasses, being greater at small and intermediate sized kills than at large ones. In the presence of females, mild intramale aggression was only seen within 1 of 7 coalitions. Free-living females showed similar rates of behavior in the presence of different numbers of males, aside from more frequent growling at large groups. These findings suggest that captive institutions should be less nervous about housing male cheetahs together and introducing females to groups of males for purposes of breeding. © 1993 Wiley-Liss, Inc.     

Reproductive Parameters of Female<Emphasis Type="Italic">Pan paniscus</Emphasis> and <Emphasis Type="Italic">P. troglodytes</Emphasis>: Quality versus Quantity

We investigated intra- and interspecific differences in life history and reproductive parameters in bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). We compare the parameters of wild and captive females in order to shed light on the influence of habitat or specific differences or both on reproduction. We present new and additional information on reproductive parameters from captive bonobos and chimpanzees. Captive chimpanzees birth more live offspring and have a shorter interbirth interval, but experience higher infant mortality than captive bonobos. Although captive bonobo females tend to start reproduction at a younger age than chimpanzees, this is effectively only so for wild-born females of both species. Ultimately both species reach the same rate of production of offspring surviving to 5 yr. These results contrast with data from the wild. Wild bonobos tend to have higher reproductive success, a higher fertility rate and a shorter interbirth interval than wild chimpanzees. Reproduction is similar for wild and captive bonobos, which suggests that they are producing at their maximum under both conditions. Overall captive chimpanzees perform better than their wild conspecifics, probably because of lower feeding competition. Infant survival is the only specific difference not affected by captivity. Bonobo infants survive better, which suggests that chimpanzee infants are more at risk. We argue that the interspecific variation in reproductive parameters in captivity is related to the different influence of captivity on reproduction and different pressures of external sources of infant and juvenile mortality.     

Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator

Precise measures of phenology are critical to understanding how animals organize their annual cycles and how individuals and populations respond to climate-induced changes in physical and ecological stressors. We show that patterns of core body temperature (T _b) can be used to precisely determine the timing of key seasonal events including hibernation, mating and parturition, and immergence and emergence from the hibernacula in free-living arctic ground squirrels (Urocitellus parryii). Using temperature loggers that recorded T _b every 20 min for up to 18 months, we monitored core T _b from three females that subsequently gave birth in captivity and from 66 female and 57 male ground squirrels free-living in the northern foothills of the Brooks Range Alaska. In addition, dates of emergence from hibernation were visually confirmed for four free-living male squirrels. Average T _b in captive females decreased by 0.5–1.0°C during gestation and abruptly increased by 1–1.5°C on the day of parturition. In free-living females, similar shifts in T _b were observed in 78% (n = 9) of yearlings and 94% (n = 31) of adults; females without the shift are assumed not to have given birth. Three of four ground squirrels for which dates of emergence from hibernation were visually confirmed did not exhibit obvious diurnal rhythms in T _b until they first emerged onto the surface when T _b patterns became diurnal. In free-living males undergoing reproductive maturation, this pre-emergence euthermic interval averaged 20.4 days (n = 56). T _b-loggers represent a cost-effective and logistically feasible method to precisely investigate the phenology of reproduction and hibernation in ground squirrels.     

Captive rearing of Puget blue butterflies (Icaricia icarioides blackmorei) and implications for conservation

The use of captive rearing to promote recovery of endangered butterflies has substantially increased over the last decade. These programs have the potential to play a significant role in butterfly population recovery, but the effects of captive conditions are poorly understood and rarely are traits of captive individuals assessed relative to traits in their founding populations. To develop rearing protocols and investigate possible effects of captive conditions, we reared Puget blue butterflies (Icaricia icarioides blackmorei), a subspecies closely related to the endangered Fender’s blue (I. i. fenderi) which is limited to Oregon, USA. We reared individuals from two wild populations in Washington, USA to investigate two approaches for egg collection (collect eggs in the wild vs. collect eggs from adult females which were brought to a greenhouse for oviposition) and three diapause environments (in indoor facilities at two independent locations vs. outdoors in enclosures). Survival from egg to adult was similar across all captive groups which survived past diapause and was less than 10%. Captive reared individuals were lighter and had smaller wings and shorter body lengths than their founding populations for both sites. Based on our findings, we recommend that rearing programs compare characteristics of reared individuals to individuals from the founding population to quantify possible effects of captive conditions, diapause individuals in natural environments, and for programs with survival rates similar to rates in the wild, consider alternatives to augment declining populations and reintroduce historic ones.     

Vaginal estrus in unmated Belding's ground squirrels

Belding's ground squirrels are seasonally breeding rodents that have a single annual mating season (ca. 3 weeks long) which begins shortly after their vernal emergence from a 7-month period of hibernation. In this study, changes in vaginal estrus were assessed among unmated captive females. Following a 7-month period in a coldroom, vaginal lavages were taken daily to monitor changes in estrous condition. Females were in vaginal estrus within 24-48 hr of removal from the coldroom. Rather than exhibiting repeated cycles, adults (greater than or equal to 2 years old) remained in prolonged estrus (typically 3-4 weeks, but 8-10 weeks in some cases), whereas yearlings exhibited similar but shorter and possibly periodic changes in vaginal condition. The difference between the two age classes persisted in a second year of testing, indicating that the preadult status of yearlings (in the first year of testing) did not primarily account for the difference. In another experiment, removal from the coldroom was delayed for 24 days relative to adults removed at a time coincident with emergence from hibernation of free-living females. The "delayed" adults showed persistent vaginal estrus for a shorter total duration, such that both groups reached anestrus at approximately the same time. This implies that the latency to anestrus is not simply a fixed period from the time of removal from the coldroom.     

Reproductive life history of South African cheetahs (Acynonyx jubatus jubatus) at the San Diego Zoo Wild Animal Park, 1970–2005

We analyzed 35 years of data from a captive breeding program of cheetahs to determine basic reproductive life history characteristics of females. Breeding females ranged in age from 2.7–10.5 years. Sixteen females and over 13 males produced 129 cubs in 36 litters, with an average litter size of 3.6. Older females produced significantly fewer cubs per litter than younger females, but cub survivorship was comparable across female ages. Sex ratio was balanced at birth and 71% of infants survived the weaning period. Given that the reproductive output of captive cheetahs in our study is similar to that in other zoologic institutions and to cheetahs in the wild, we suggest that reproductive deficits in captive cheetahs arise from the inability of some pairs to breed, due to a lack of mating preference, rather than from a species‐wide problem. Zoo Biol 0:1–8, 2006. © 2006 Wiley‐Liss, Inc.     

How Rearing History Affects Alarm-call Responses of Belding's Ground Squirrels (Spermophilus beldingi, Sciuridae)

Juvenile, but not adult, Belding’s ground squirrels (Spermophilus beldingi) exhibit markedly different responses to alarm calls as a function of their environment. Compared with same-aged, free-living juveniles, captive juveniles (housed in large outdoor enclosures) are more likely to respond to playbacks, to exhibit more exaggerated initial responses (e.g. enter a burrow vs. freeze) and to remain alert longer following playbacks of alarm and non-alarm calls. Two studies were conducted to identify the factors contributing to these response differences. Postemergent rearing environments (such as the opaque enclosure walls that limited visual and auditory stimulation in captivity, or the increased number of conspecifics and natural alarm calls that free-living juveniles experienced) could not account for the majority of response differences between captive and free-living juveniles (Study 1). To determine if the attenuated responses of free-living juveniles were due to foraging pressures, we compared the behaviours of food-provisioned captive juveniles with those of non-provisioned captive juveniles. Although sample sizes were small, no differences were evident in the development or expression of responses as a function of foraging pressure. Next, the development of captive juveniles was compared with that of juveniles reared in the field but housed in captivity after emergence (Study 2). Differences in the response patterns of field-reared and captive-reared animals matched the differences reported previously, as the responses of field-reared animals observed in captivity mirrored those of free-living juveniles that remained in the field. Thus, the differences in alarm-call responses originally observed between captive and free-living juveniles are attributed to their pre-emergent, but not post-emergent, rearing histories. Captive pups experienced levels of auditory, visual, tactile, and olfactory stimulation that were greater than those typically experienced by free-living pups. The increased exposure to conspecific alarm calls may have primed captive pups to respond more often and more intensely to the auditory stimuli they heard as juveniles. Sensitivity to early rearing environments may be adaptive for young ground squirrels if it facilitates the development of antipredator behaviour patterns that are appropriate for the local predator environment (e.g. openness of habitat, frequency of predators, availability of refuges).     

Sexual behaviour of male and female tammar wallabies (Macropus eugenii) at post-partum oestrus

This study describes the sexual behaviour of the adult male and female tammar wallaby from the time a female gives birth to the end of post-partum oestrus. Eleven females were continuously observed from around the time of birth until up to 3 h after the last observed mating attempt. Males began to associate with females from around the time of birth, thus females appear to be attractive to males at, but not prior to parturition. Females subsequently allowed males to mate with them from 1.3±0.8h (mean±S.D.) post-partum, although the first ejaculation was delayed until 1.8±0.8h after birth owing to intense intermale aggression directed towards any male which attempted to mate with an oestrous female. Mating chases, in which a post-partum female was pursued by several males, were observed from 1.3±0.8h post-partum. All of this mating activity usually occurred within the first 6h after birth.     

A condition dependent link between testosterone and disease resistance in the house finch.

Testosterone has recently been proposed as a link between male quality and health and the expression of sexual traits. We investigated the relationship between testosterone and measures of the individual condition and health of males in a natural population of house finches (Carpodacus mexicanus). We also conducted a captive experiment in order to test for the effects of testosterone on resistance to coccidia, which is a common parasite of house finches. Free-living males in better condition had higher testosterone levels and lower corticosterone levels than free-living males in poor condition. In our captive experiment, increased testosterone accelerated the rate of coccidial infection as compared with sham-implanted or gonadectomized males. Although the differences were not significant, free-living males infected with coccidia had lower levels of testosterone and higher levels of corticosterone than males that were not infected. Thus, experimentally elevating testosterone levels in captive males resulted in a higher percentage of infected males, while free-living males with coccidial infection had low testosterone levels. This apparent discrepancy between captive and free-living males in the association of testosterone and disease may be explained by the condition dependence of testosterone. These results suggest that the testosterone-dependent sexual traits reliably indicate male overall condition and health and, thus, females could benefit from assessing potential mates based on these traits.     

Post-partum events and fertility control in Kinshasa, Za?re

Contraceptive prevalence surveys from sub-Saharan Africa typically show low rates of method use. The current study of one zone in Kinshasa, Za?re, provides a more detailed view of fertility control in an urban population by examining the relative duration of breast-feeding, amenorrhoea and sexual abstinence during the post-partum period. While motivations to prevent pregnancy remain high until the youngest child is over 24 months, the average duration of abstinence is only 4 months. This paper describes the methods women use to avoid pregnancy and the changes over the post-partum period.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.