Ronald R. Swaisgood

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.

Reproductive cycle length and pregnancy in the southern white rhinoceros (Ceratotherium simum simum) as determined by fecal pregnane analysis and observations of mating behavior

Pregnancy and the reproductive cycle were monitored in 13 captive southern white rhinoceros (Ceratotherium simum simum) by measuring progesterone metabolites in fecal extracts and by observing behavior patterns. Fecal hormones were measured using a monoclonal antibody produced against 4-pregnen-11-o1-3,20-dione hemisuccinate:BSA. Several subjects exhibited flat or erratic endocrine profiles, but we found evidence for 17 reproductive cycles in five females. Mating behavior coincided with nadirs in pregnane concentrations. These cycles appeared to fall into two general categories: those of approximately 1 month in duration (Type I: X¯ ± SEM = 35.4± 2.2 days; n = 10) and those lasting approximately 2 months (Type II: 65.9± 2.4 days; n = 7). Interluteal phase lengths were similar for the two cycle types, but Type II cycles were characterized by extended luteal phases lasting more than twice as long as Type I luteal phases. Because Type I cycles predominated in our data and because evidence suggests that some Type II cycles may be aberrant, we argue that these approximately monthly cycles represent the typical reproductive cycle for this species. Three females became pregnant during the course of the study. We were able to detect pregnancy by approximately 3 months post-breeding, as indicated by sustained pregnane concentrations markedly higher than nonpregnant luteal phase concentrations. These data help to characterize important reproductive events of this species and should be useful for captive breeding efforts for this threatened species. Zoo Biol 18:111–127, 1999.

Old-growth forest is what giant pandas really need

Giant pandas (Ailuropoda melanoleuca) are an iconic conservation species, but despite significant research effort, do we understand what they really need? Estimating and mapping suitable habitat play a critical role in conservation planning and policy. But if assumptions about ecological needs are wrong, maps with misidentified suitable habitat will misguide conservation action. Here, we use an information-theoretic approach to analyse the largest, landscape-level dataset on panda habitat use to date, and challenge the prevailing wisdom about panda habitat needs. We show that pandas are associated with old-growth forest more than with any ecological variable other than bamboo. Other factors traditionally used in panda habitat models, such as topographic slope, are less important. We suggest that our findings are disparate from previous research in part because our research was conducted over a larger ecological scale than previous research conducted over more circumscribed areas within individual reserves. Thus, extrapolating from habitat studies on small scales to conservation planning on large scales may entail some risk. As the Chinese government is considering the renewal of its logging ban, it should take heed of the pandas dependency on old growth.

The highs and lows of chemical communication in giant pandas (Ailuropoda melanoleuca): effect of scent deposition height on signal discrimination

Abstract. The giant pandas (Ailuropoda melanoleuca) social system is not well known, but it is clear that competition and avoidance characterizes social interaction for this solitary species throughout most of the year. Chemical communication appears to play a major role in structuring these interactions. Pandas adopt four distinct marking postures that deposit anogenital gland secretions or urine at varying heights: squat, reverse, legcock and handstand. In this experiment we tested the behavioral responses of 28 captive pandas belonging to all age-sex groups to conspecific odors placed to mimic the height of these postures. We tested three odor stimuli: male urine, and male and female glandular secretions. In all cases, pandas spent more time investigating higher odors than lower odors, suggesting that pandas place more importance on gathering information about individuals that adopt elevated postures. Pandas, particularly subadult males, also showed evidence of avoiding areas where adult male urine was deposited to mimic the handstand posture. Based on these and other findings, we propose that elevated postures in pandas may function to communicate competitive ability and possibly aggressive intent. Height of odor deposition, especially in the handstand posture, may be associated with body size, a major determinant of competitive ability. Selection may favor signalers that capitalize on the assessment activities of assessors by depositing scents to emphasize height cues. If such signals of competitive ability are used to mediate aggressive interactions, subsequent selection may favor their use only when the signaler is prepared to escalate in a contest.

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.

Odor familiarity and female preferences for males in a threatened primate, the pygmy loris Nycticebus pygmaeus: applications for genetic management of small populations

Here we use sexual selection theory to develop a logistically simple, yet effective, method for the manipulation of female reproductive behavior for conservation goals. Mate choice leading to nonrandom mating patterns can exacerbate the loss of genetic diversity in small populations. On theoretical grounds, females should choose high-quality mates. A prediction stemming from chemical communication theory is that competitive males will be better able to saturate an area with scent marks. If this is true, females should mate preferentially with males whose odors they encounter most frequently. We tested this hypothesis with the pygmy loris, Nycticebus pygmaeus, a threatened and poorly studied nocturnal prosimian. For several weeks females were exposed repeatedly to the urine from a particular male, and were then allowed to choose between a male whose odors were familiar and one whose odors were novel. Females showed an unusually strong preference for the familiar-odor male, as indicated by several behavioral measures of mate preference. Conservation managers can use this method as a tool to obtain reproductive pairings that will maximize genetic compatibility and diversity. For example, unsuccessful males may be given the opportunity to reproduce. In captive populations, studbook managers often select pairs in order to optimize outbreeding, but these selected pairings may not coincide with the preferences of the individual animals involved. Although several authors have made theoretical arguments for manipulating mate choice for conservation, this is a novel test of a proximate mechanism that can be manipulated, cultivating applications rather than mere implications.

Reserve Size, Conspecific Density, and Translocation Success for Black Rhinoceros

Abstract Fighting and accidental injury commonly cause black rhinoceros (rhino; Diceros bicornis) death after release. Smaller reserves and higher conspecific density after release (release density) might increase a rhinos encounter rate with hazards like fenced boundaries and conspecifics. We conducted a science-by-management experiment on the influence of reserve size and release density on rates of movement, association, and injury and death amongst 39 black rhinos during the first 100 days after their release into 4 Namibian and 8 South African reserves ranging in size from 670 ha to 45,000 ha. Association rates were negatively related to reserve size and positively correlated with release density. There was also a negative relationship between the proportion of the reserve traversed by individual rhinos and reserve size. In reserves ≥18,000 ha association rates were consistently zero but became elevated in reserves ≤11,500 ha and at release densities ≤9 km2/rhino. Daily displacement did not increase with increasing reserve size >8,500 ha but in smaller reserves daily displacements indicated higher encounter rates by released rhinos with fenced boundaries. Three rhinos received fight-related injuries requiring intervention and 2 of 4 deaths were fight-related. All injuries and 3 deaths occurred in reserves ≤11,500 ha. Model selection based on Akaikes second-order Information Criterion indicated that the parameter release density alone best explained mortality risk. Traditionally considered risk factors, rhino sex, age, and presence of resident conspecifics, were superseded by the risk posed by releases into smaller reserves. Reserves ≤11,500 ha and release densities ≤9 km2/rhino pose an increasing risk to rhino survivorship and so larger reserves and lower densities than these should be favored as release sites.

Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase

Although female mammal vocal behaviour is known to advertise fertility, to date, no non-human mammal study has shown that the acoustic structure of female calls varies significantly around their fertile period. Here, we used a combination of hormone measurements and acoustic analyses to determine whether female giant panda chirps have the potential to signal the callers precise oestrous stage (fertile versus pre-fertile). We then used playback experiments to examine the response of male giant pandas to female chirps produced during fertile versus pre-fertile phases of the callers reproductive cycle. Our results show that the acoustic structure of female giant panda chirps differs between fertile and pre-fertile callers and that male giant pandas can perceive differences in female chirps that allow them to determine the exact timing of the females fertile phase. These findings indicate that male giant pandas could use vocal cues to preferentially associate and copulate with females at the optimum time for insemination and reveal the likely importance of female vocal signals for coordinating reproductive efforts in this critically endangered species.

Ecological scale and seasonal heterogeneity in the spatial behaviors of giant pandas

We report on the first study to track the spatial behaviors of wild giant pandas (Ailuropoda melanoleuca) using high-resolution global positioning system (GPS) telemetry. Between 2008 and 2009, 4 pandas (2 male and 2 female) were tracked in Foping Reserve, China for an average of 305 days (± 54.8 SE). Panda home ranges were larger than those of previous very high frequency tracking studies, with a bimodal distribution of space-use and distinct winter and summer centers of activity. Home range sizes were larger in winter than in summer, although there was considerable individual variability. All tracked pandas exhibited individualistic, unoriented and multiphasic movement paths, with a high level of tortuosity within seasonal core habitats and directed, linear, large-scale movements between habitats. Pandas moved from low elevation winter habitats to high elevation (>2000 m) summer habitats in May, when temperatures averaged 17.5 °C (± 0.3 SE), and these large-scale movements took <1 month to complete. The peak in panda mean elevation occurred in Jul, after which they began slow, large-scale movements back to winter habitats that were completed in Nov. An adult female panda made 2 longdistance movements during the mating season. Pandas remain close to rivers and streams during winter, possibly reflecting the elevated water requirements to digest their high-fiber food. Panda movement path tortuosity and first-passage-time as a function of spatial scale indicated a mean peak in habitat search effort and patch use of approximately 700 m. Despite a high degree of spatial overlap between panda home ranges, particularly in winter, we detected neither avoidance nor attraction behavior between conspecifics.