Donald G. Lindburg

Giant pandas discriminate individual differences in conspecific scent.

The functions and mechanisms of chemical communication are well established for many species of small mammal amenable to investigation, but systematic research is virtually absent for large, rare species. The present study marks the first systematic investigation of chemical communication in the endangered giant panda, Ailuropoda melanoleuca. Using a habituation-discrimination paradigm, we sought to determine whether giant pandas can discriminate between scents from different individuals on the basis of chemical cues afforded by female urine and male anogenital gland secretions. Pandas habituated to successive presentations of scent stimuli from a single individual, as evidenced by diminished responsiveness across five habituation trials. In the discrimination test for male anogenital gland secretions, subjects of both sexes investigated a new individuals scent significantly more than a familiar scent to which they were previously habituated. Neither sex significantly discriminated novel from habituated female urine, although a strong tendency to differentiate the stimuli was evident. We also found that the sex of the subject affected patterns of response. Females showed a significant preference for male anogenital gland secretions, whereas males investigated both types of scent stimuli equally. In general, male subjects were more responsive than females to conspecific scent, especially female urine. This study provides clear evidence that giant pandas distinguish individual odours emanating from male anogenital secretions, and implies that these odours contain individually distinctive chemical signatures. These results have implications that can be applied to the conservation and management of this species. Copyright 1999 The Association for the Study of Animal Behaviour.

A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas

Abstract With the goal of enhancing psychological well-being, we developed an environmental enrichment programme for eight subadult and six adult giant pandas, Ailuropoda melanoleuca, at the Wolong Breeding Center in Sichuan, China. We used five different enrichment items, each selected because of the different behavioural opportunities they promoted: (1) manipulable plastic objects; (2) a burlap sack full of straw; (3) spruce branches; (4) a fruitcicle (apples frozen in a large ice block); and (5) a puzzle feeder. Each subject received each of the five items on three occasions, for a total of 15 enrichment sessions over the course of the 2.5-month study period. Each enrichment session was paired with a control session in which no enrichment was present. Pandas spent significantly more time active, and displayed a greater variety of object- and nonobject-directed behaviours when enrichment was present. We also found a statistically significant reduction in the rate of and percentage of time engaged in the performance of stereotypic behaviour and behaviours indicative of feeding anticipation. This effect was maintained even when pandas were not interacting directly with an enrichment item, suggesting that enrichment had a motivational carry-over effect in the aftermath of interactions with enrichment items. These results are consistent with the ethological needs model of motivation in that opportunities to perform more natural behaviour appeared to improve motivational indices of well-being. The pandas remained responsive to enrichment across the 15 trials, providing no evidence for habituation or cross-habituation. Age proved to be an important determinant of responsiveness; for example, adults, but not subadults, displayed a significant preference for feeding enrichment. Future studies will assess whether these promising initial results are maintained throughout the lives of captive giant pandas.

Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus)

This longitudinal study addresses the relationship of cortisol excretion to ovarian activity in captive female cheetahs. A radioimmunoassay was developed and validated to measure corticoid metabolite concentrations in feces. A restraint experiment was used to demonstrate that fecal cortisol is detectable following stressful episodes. In studies of 7 females, fecal cortisol output indicated that they could be placed into 3 different categories. Females of the high-in-cortisol category (∼200 ng/g feces, n = 2) were independently rated by caretakers as the most nervous individuals in the collection (n = 24). These females appeared to be compromised in their ovarian cycling, as indicated by fecal estrogen measurements. In contrast, reproducing females fell into the low and intermediate cortisol excretion categories. A non-cycling high-cortisol female had an episodic cycle following a period of relatively low (intermediate) cortisol levels, followed by resumption of acyclicity and high cortisol excretion. Stress and reproductive failure may, therefore, be associated in the female cheetah. The close proximity of conspecifics as a potential source of stress and, consequently, suppressed ovarian activity in some females is suggested by these results. Zoo Biol 16:133–147. 1997

Discrimination of oestrous status in giant pandas ( Ailuropoda melanoleuca ) via chemical cues in urine

Giant pandas Ailuropoda melanoleuca are a solitary, seasonally mono-oestrous species, and as such are likely to rely heavily on chemical signals to co-ordinate mating efforts. Perhaps the most crucial chemosensory task facing male pandas is the assessment of female reproductive condition on the basis of chemical cues. To test for this ability, eight male and 10 female giant pandas were presented with urine from oestrous and non-oestrous females. Males but not females displayed a significant investigatory preference for oestrous over non-oestrous female urine, as indicated by sniffing and flehmen. Males also investigated, displayed flehmen, and licked female urine more than did females. These findings indicate that female urine contains chemical cues permitting discrimination of oestrous status, and probably serves a reproductive advertisement function. The prevalence of flehmen and licking by males suggests that males may rely on the vomeronasal organ to assess female reproductive condition. Female odours may play an important role in the reproductive behaviour of male giant pandas and, therefore, may have implications for captive-breeding programmes.

Carcass Feeding of Captive Cheetahs (Acinonyx jubatus): the Effects of a Naturalistic Feeding Program on Oral Health and Psychological Well-being

Abstract Based on preliminary observations of 15 cheetahs at the San Diego Wild Animal Park, a protocol of behaviors associated with feeding was devised. Five animals were then acclimated to videotaping from which comparisons of feeding on commercial and carcass diets were made. Improved appetites, longer feeding bouts and a greater possessiveness of food characterized the carcass-fed animals. Although the commercial diet is nutritionally balanced, these differences indicate that certain non-nutritive requirements are important to psychological health. In addition, the dental abnormalities and oral infections that are found in the captive population could be an indication of the importance of food texture. By recognizing the importance of food texture, flavor and temperature to the effort expended and interest demonstrated in feeding by captive cheetahs, we may enhance their physical and psychological well-being.

The reproductive strategy of giant pandas (Ailuropoda melanoleuca): infant growth and development and mother–infant relationships

Reproductive activities of six giant panda females ( Ailuropoda melanoleuca ) living in the Qinling Mountains of China (Shaanxi Province) were recorded from 1989 into early 1995. Data on mating and birth dates, litter size, cub sex and den use were collected for three of the pandas. At this site, pregnant females migrated to lower elevations in advance of other pandas to seek dens for birthing. One dam was videotaped in the den with her cub from birth to the end of the denning phase at 94 days of age. This cub was repeatedly handled during the dams absences to obtain data on development and weight. During the early part of the denning phase, the cub was maintained on the dams body virtually continuously. Post-partum fasting for up to 3 weeks was noted. Dams invariably moved cubs to new dens three or four times during the birth season. By the time cubs left the den at about 3–4 months, they were fully furred and capable of surviving winter temperatures without further shelter. Reproductive parameters for the wild population fell within the range of values for captive pandas, based on information in the literature and in the giant panda studbook. The combined data on length of gestation, intervals between births, litter size and weight, infant development, and reproductive life span reveal a range of life-history variables that strongly resemble the Ursidae.

Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation

Several recent studies indicate that primate species may differ in behavioral, and in some instances physiological, responses to social manipulations. These differences in response dispositions have been interpreted as being based on temperamental differences among species. This report extends previous comparative studies of macaques by describing behavioral contrasts observed between males of two macaque species, lion-tailed and cynomolgus macaques, in response to social manipulations. Males were exposed to a mirror, then visually exposed to conspecific neighbors in all pairwise combinations, and then formed into conspecific social groups. Urine samples were collected in the pairing and group formation conditions for cortisol assay. The cynomolgus demonstrated more affiliative behavior than the lion-tails in all conditions, while the lion-tails tended to exhibit more aggressive behavior. Following group formation cortisol values showed a decreasing trend in the cynomolgus, but not in the lion-tails. The cynomolgus rapidly adapted to group living and relations between them were primarily affiliative. In contrast, no affiliative behavior was ever observed in the lion-tail group, which appeared to be highly stressed by group living and was eventually disbanded.

A preliminary study of the effects of ecologically relevant sounds on the behaviour of captive lowland gorillas

Abstract This exploratory study evaluated the effects of ecologically relevant sounds on captive lowland gorillas (Gorilla gorilla gorilla), housed in the night quarters adjacent to their new exhibit at the San Diego Zoo. The behaviour of four western lowland gorillas was sampled using remote videotaping under each of four noise conditions associated with captive housing (quiet, ventilation on, bonobo vocalization playbacks and caretaker sounds) and each of two sound conditions (rain forest sounds ‘off’, rain forest sounds ‘on’). Significant differences in behaviour across noise conditions were found; these differences were ameliorated for infants, but only partially for adults by the rain forest sounds. The two adults responded to the rain forest sounds with increased agitation. The preliminary nature of these results is discussed.

Seasonal and diurnal dynamics of glucocorticoids and behavior in giant pandas

Abstract Because of the suppressive effect of stress on reproduction and health, it is important to evaluate potential stressors that may compromise captive breeding programs for endangered species. However, behavioral and physiological measures of stress are sometimes difficult to interpret, and their relationship to stress can be obscured by factors unrelated to stress, such as seasonal and diurnal patterns. Here we present findings for daily and seasonal variation in glucocorticoid (GC) secretion and behavior from a 6-year study of 2 giant pandas (Ailuropoda melanoleuca). In the American black bear (Ursus americanus), seasonal patterns of corticoid secretion are putatively linked to metabolic demands of hibernation. Although pandas do not hibernate, we have found a similar pattern of GC dynamics. Using radioimmunoassay of urinary GC metabolites, we found seasonal variation in GC levels in an adult female and an adult male panda. As in black bears, winter and spring GC levels were significantly higher than summer levels. Additionally, in the female, GC levels during the period of parental care and lactation were higher, regardless of calendar season, than during other periods. Diurnal patterns were also detected in both the female and male panda, with elevated GCs in the morning sample. However, these diurnal patterns were not evident during the fall and summer months. Daily levels of several behaviors potentially indicative of stress also varied significantly with season in both male and female. Additionally seasonal dynamics of feeding behavior were documented. In the female, periods of elevated and diminished appetite were associated with embryonic diapause and post-implantation, respectively. The male had elevated feeding during the fall. Although these patterns are instructive for comparison with other species, we urge caution because our limited sample size does not allow us to extrapolate beyond the individuals studied.

A method for encouraging maternal care in the giant panda.

We developed a method to facilitate maternal care in a giant panda (Ailuropoda melanoleuca) female that rejected her cub immediately after parturition. After removal of the cub, the female was systematically exposed to a regime of infant-related stimuli, including a surrogate toy panda, accompanied by infant vocalizations and urine, and the mothers own milk. The female displayed several measures of maternal behavior toward the surrogate, for example, spending 61% of her time holding the surrogate in positions typical for the species. There was some evidence that maternal proficiency increased across the 4 weeks of the experiment. Results also indicate that the female was responsive to both infant vocalizations and urine, but not milk. After a transitional period in which we assisted the female in her efforts to nurse and groom the infant, all maternal care-giving responsibilities were returned to the mother. Over the next 3 months, the pattern of maternal care followed the species-typical course of declining mother-infant contact, grooming, overall interaction time, and responsiveness to the cubs vocalizations. This study marks the first successful reunification of a giant panda mother with an infant separated at birth and, it is hoped, will serve as a model for similar efforts elsewhere. Zoo Biol 19:53–63, 2000.