Hemin Zhang

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.

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.

Potential Chemosignals in the Anogenital Gland Secretion of Giant Pandas, Ailuropoda melanoleuca, Associated with Sex and Individual Identity

With a combination of dichloromethane extraction and analysis by gas chromatography–mass spectrometry (GC-MS), we found 39 compounds (corresponding to 38 GC peaks) in the anogenital gland secretion (AGS) of captive adult giant pandas, Ailuropoda melanoleuca, during the non-mating season. In addition to indole, squalene, and some of the straight-chain fatty acids that had been characterized previously from the AGS of giant pandas, we identified several new compounds such as decenal, two isomers of decadienal, phenylacetic acid, 5-methylhydantoin, hydroquinone, phenylpropanoic acid, and erucic acid. Quantitative comparison of the relative abundances of the 20 main GC peaks revealed that 5-methylhydantoin, indole, and erucic acid are putative female pheromones, whereas squalene and hydroquinone are putative male pheromones. In addition to the presence of a few individual-specific compounds, the relative abundances of most of the 21 constituents varied more among individuals than within individuals. This suggests that individual identity might be coded in both digital and analog form. The chemical composition of different AGS samples from the same pandas consistently displayed a minimum cluster distance, much smaller than that between samples from different individuals in a hierarchical linkage cluster (average linkage) dendrogram. Our results indicate that the AGS might contain an “odor fingerprint.” Although putative sex pheromones such as squalene and erucic acid should be assessed further by bioassay, our study suggests that synthetic chemosignals might be useful in modulating the behavior and physiology of giant pandas.

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.

Free mate choice enhances conservation breeding in the endangered giant panda.

Conservation breeding programmes have become an increasingly important tool to save endangered species, yet despite the allocation of significant resources, efforts to create self-sustaining populations have met with limited success. The iconic giant panda (Ailuropoda melanoleuca) embodies the struggles associated with ex situ species conservation. Here we show that behavioural mate preferences in giant pandas predict reproductive outcomes. Giant pandas paired with preferred partners have significantly higher copulation and birth rates. Reproductive rates increase further when both partners show mutual preference for one another. If managers were to incorporate mate preferences more fully into breeding management, the production of giant panda offspring for Chinas reintroduction programme might be greatly expedited. When extended to the increasing numbers of species dependent on ex situ conservation breeding to avoid extinction, our findings highlight that mate preference and other aspects of informed behavioural management could make the difference between success and failure of these programmes.

Enhancing captive breeding in giant pandas (Ailuropoda melanoleuca): maintaining lactation when cubs are rejected, and understanding variation in milk collection and associated factors.

From 1997 to 2002, a female giant panda (Ailuropoda melanoleuca) was artificially stimulated and lactation was maintained, after her neonates were removed due to the females inability to provide maternal care. Milk samples were collected and the amount of milk collected was quantified. The lactation curve of this animal was estimated based on the Gamma function: Y(t)=at(b)e(-ct). The amount of milk collected showed significant, positive relationships with the number of days after parturition both in 1999 and in the whole study period from 1998 to 2002. This females lactation curves fit the type I pattern of a typical mammalian lactation curve. Daily milk collection (g) during the first 30 days after parturition, and from 31 to 60 days after parturition, showed a consistent pattern with one peak at around 8:00 hr. More milk was collected during the latter period than during the former period. The amount of milk (g) collected on mucus excretion days was significantly less than that on days after mucus excretion had ended, yet no significant difference was found between milk collected one day before mucus days and on mucus days, or between milk collected one day before and one day after mucus days. Mucus excretion from the gastrointestinal tract significantly impacted the amount of milk collected. The results from this study may aid the captive propagation and conservation of giant pandas and other endangered and rare captive mammal species.

Sound transmission in a bamboo forest and its implications for information transfer in giant panda ( Ailuropoda melanoleuca ) bleats

Although mammal vocalisations signal attributes about the caller that are important in a range of contexts, relatively few studies have investigated the transmission of specific types of information encoded in mammal calls. In this study we broadcast and re-recorded giant panda bleats in a bamboo plantation, to assess the stability of individuality and sex differences in these calls over distance, and determine how the acoustic structure of giant panda bleats degrades in this species’ typical environment. Our results indicate that vocal recognition of the caller’s identity and sex is not likely to be possible when the distance between the vocaliser and receiver exceeds 20u2009m and 10u2009m, respectively. Further analysis revealed that the F0 contour of bleats was subject to high structural degradation as it propagated through the bamboo canopy, making the measurement of mean F0 and F0 modulation characteristics highly unreliable at distances exceeding 10u2009m. The most stable acoustic features of bleats in the bamboo forest environment (lowest % variation) were the upper formants and overall formant spacing. The analysis of amplitude attenuation revealed that the fifth and sixth formant are more prone to decay than the other frequency components of bleats, however, the fifth formant still remained the most prominent and persistent frequency component over distance. Paired with previous studies, these results show that giant panda bleats have the potential to signal the caller’s identity at distances of up to 20u2009m and reliably transmit sex differences up to 10u2009m from the caller, and suggest that information encoded by F0 modulation in bleats could only be functionally relevant during close-range interactions in this species’ natural environment.

Blood Lead Levels in Captive Giant Pandas

Fifteen giant pandas (Ailuropoda melanoleuca) from the Chinese Conservation and Research Center for the Giant Panda (CCRCGP) in Bifengxia, Sichuan, China were analyzed for blood lead concentrations (Pb-B) during the 2017 breeding season. Thirteen of the 15 bears showed Pb-B below the method detection limit (MDL) of 3.3xa0µg/dL. The two remaining bears, although above the MDL, contained very low concentrations of lead of 3.9 and 4.5xa0µg/dL. All 15 giant pandas in this analysis had Pb-B concentrations that were within normal background concentrations for mammals in uncontaminated environments. For a threatened species, whose native country is plagued by reports of extremely high air pollution, our findings suggest that giant pandas at the CCRCGP are not absorbing lead at concentrations that would adversely affect their health.