• Chemical signals of age, sex and identity in black rhinoceros

      Linklater, W. L.; Mayer, K.; Swaisgood, Ronald R. (2013)
      Olfactory communication may be particularly important to black rhinoceros, Diceros bicornis, because they are solitary living and have comparatively poor eyesight but their populations are structured by inter-and intrasexual relationships. Understanding olfactory functions and processes might achieve better conservation management but their study in rhinoceros remains anecdotal or descriptive….
    • Chemical signatures of femoral pore secretions in two syntopic but reproductively isolated species of Galápagos land iguanas (Conolophus marthae and C. subcristatus)

      Colosimo, Giuliano; Di Marco, Gabriele; D’Agostino, Alessia; Gismondi, Angelo; Vera, Carlos A.; Gerber, Glenn P.; Scardi, Michele; Canini, Antonella; Gentile, Gabriele (Springer Science and Business Media LLC, 2020)
      The only known population of Conolophus marthae (Reptilia, Iguanidae) and a population of C. subcristatus are syntopic on Wolf Volcano (Isabela Island, Galápagos). No gene flow occurs suggesting that effective reproductive isolating mechanisms exist between these two species. Chemical signature of femoral pore secretions is important for intra- and inter-specific chemical communication in squamates. As a first step towards testing the hypothesis that chemical signals could mediate reproductive isolation between C. marthae and C. subcristatus, we compared the chemical profiles of femoral gland exudate from adults caught on Wolf Volcano. We compared data from three different years and focused on two years in particular when femoral gland exudate was collected from adults during the reproductive season. Samples were processed using Gas Chromatography coupled with Mass Spectrometry (GC–MS). We identified over 100 different chemical compounds. Non-Metric Multidimensional Scaling (nMDS) was used to graphically represent the similarity among individuals based on their chemical profiles. Results from non-parametric statistical tests indicate that the separation between the two species is significant, suggesting that the chemical profile signatures of the two species may help prevent hybridization between C. marthae and C. subcristatus. Further investigation is needed to better resolve environmental influence and temporal reproductive patterns in determining the variation of biochemical profiles in both species.
    • Chilled frogs are hot: hibernation and reproduction of the Endangered mountain yellow-legged frog Rana muscosa

      Santana, Frank E.; Swaisgood, Ronald R.; Lemm, Jeffrey M.; Fisher, Robert N.; Clark, Rulon W. (2015)
      In the face of the sixth great extinction crisis, it is imperative to establish effective breeding protocols for amphibian conservation breeding programs. Captive efforts should not proceed by trial and error, nor should they jump prematurely to assisted reproduction techniques, which can be invasive, difficult, costly, and, at times, counterproductive. Instead, conservation practitioners should first look to nature for guidance, and replicate key conditions found in nature in the captive environment, according to the ecological and behavioral requirements of the species. We tested the effect of a natural hibernation regime on reproductive behaviors and body condition in the Endangered mountain yellow-legged frog Rana muscosa. Hibernation had a clear positive effect on reproductive behavior, manifesting in vocal advertisement signaling, female receptivity, amplexus, and oviposition. These behaviors are critical components of courtship that lead to successful reproduction. Our main finding was that captive R. muscosa require a hibernation period for successful reproduction, as only hibernated females produced eggs and only hibernated males successfully fertilized eggs. Although hibernation also resulted in a reduced body condition, the reduction appeared to be minimal with no associated mortality. The importance of hibernation for reproduction is not surprising, since it is a major component of the conditions that R. muscosa experiences in the wild. Other amphibian conservation breeding programs can also benefit from a scientific approach that tests the effect of natural ecological conditions on reproduction. This will ensure that captive colonies maximize their role in providing genetic reservoirs for assurance and reintroduction efforts.
    • Do opposites attract? Effects of personality matching in breeding pairs of captive giant pandas on reproductive success

      Martin-Wintle, Meghan S.; Shepherdson, David; Zhang, Guiquan; Huang, Yan; Luo, Bo; Swaisgood, Ronald R. (2017)
      Successful and cost-effective conservation breeding programs rely largely on animals doing what should come naturally: mate & reproduce. Behavioral management, especially that targeting mate compatibility and choice, will be important to achieve breeding goals efficiently. The endangered giant panda, Ailuropoda melanoleuca, was once notorious for its poor reproductive performance in captivity. Although the panda breeding program has experienced great improvement in recent years, we hypothesized that a better understanding of the role personality traits play in mating behavior could further improve reproductive performance. We used animal caretaker surveys and novel object tests to characterize pandas according to several personality traits—including exploratory, aggressiveness, excitability, fearfulness, and general activity—and tested how variation in these traits influenced mate compatibility and offspring production. Our findings indicate that specific combinations of personality traits showed better reproductive performance than others. Sometimes personality trait similarity enhanced reproduction and sometimes it impaired reproduction, depending on the trait. For example, Excitable males paired with Low-Excitable females had better reproductive outcomes, but pairs with Low-Fearful males regardless of the female's Fearfulness performed better. Males that were more Aggressive than their female partner were more likely to mate and produce cubs than when the female had a higher level of Aggressiveness than the male. Applying these results to breeding management strategies should result in higher reproductive rates and the production of more candidates for China's panda reintroduction program. These results highlight the potential importance of associative mating patterns based on personality for conservation breeding programs for a large number of other species.
    • Dynamics of male-female multimodal signaling behavior across the estrous cycle in giant pandas (Ailuropoda melanoleuca)

      Owen, Megan A.; Swaisgood, Ronald R.; McGeehan, L.; Zhou, X.; Lindburg, Donald G. (2013)
      Giant panda courtship behavior includes multimodal signaling assemblages consisting of olfactory, vocal, and postural elements. While signaling is generally conspicuous, successful copulation is inconsistently achieved in captivity, even when female behavioral and physiological data indicate that ovulation is imminent. We set out to characterize these complex patterns of social behavior by observing interactions between 26 unique pairs of giant pandas housed in adjoining pens throughout the females' reproductive cycle....
    • Evidence for dominant males but not choosy females in an insular rock iguana

      Moss, Jeanette B.; Gerber, Glenn P.; Schwirian, Aumbriel; Jackson, Anna C.; Welch, Mark E. (2018)
      In natural populations susceptible to inbreeding depression, behaviors such as female promiscuity and disassortative mating may enhance the production of outbred progeny and help maintain genetic variation at the population-level. However, empirical tests of such hypotheses have largely focused on mating systems in which female choice is known to play a large role....
    • Free mate choice enhances conservation breeding in the endangered giant panda

      Martin-Wintle, Meghan S.; Shepherdson, David; Zhang, Guiquan; Zhang, Hemin; Li, Desheng; Zhou, Xiaoping; Li, Rengui; Swaisgood, Ronald R. (2015)
      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 China’s 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.
    • Highly polymorphic colour vision in a New World monkey with red facial skin, the bald uakari Cacajao calvus

      Corso, Josmael; Bowler, Mark; Heymann, Eckhard W.; Roos, Christian; Mundy, Nicholas I. (2016)
      Colour vision is highly variable in New World monkeys (NWMs). Evidence for the adaptive basis of colour vision in this group has largely centred on environmental features such as foraging benefits for differently coloured foods or predator detection, whereas selection on colour vision for sociosexual communication is an alternative hypothesis that has received little attention. The colour vision of uakaris (Cacajao) is of particular interest because these monkeys have the most dramatic red facial skin of any primate, as well as a unique fission/fusion social system and a specialist diet of seeds. Here, we investigate colour vision in a wild population of the bald uakari, C. calvus, by genotyping the X-linked opsin locus. We document the presence of a polymorphic colour vision system with an unprecedented number of functional alleles (six), including a novel allele with a predicted maximum spectral sensitivity of 555 nm. This supports the presence of strong balancing selection on different alleles at this locus. We consider different hypotheses to explain this selection. One possibility is that trichromacy functions in sexual selection, enabling females to choose high-quality males on the basis of red facial coloration. In support of this, there is some evidence that health affects facial coloration in uakaris, as well as a high prevalence of blood-borne parasitism in wild uakari populations. Alternatively, the low proportion of heterozygous female trichromats in the population may indicate selection on different dichromatic phenotypes, which might be related to cryptic food coloration. We have uncovered unexpected diversity in the last major lineage of NWMs to be assayed for colour vision, which will provide an interesting system to dissect adaptation of polymorphic trichromacy.
    • Influence of season and social context on male giant panda (Ailuropoda melanoleuca) vocal behaviour

      Charlton, Benjamin D.; Owen, Megan A.; Zhou, Xiaoping; Zhang, Hemin; Swaisgood, Ronald R. (2019)
      Documenting the different social and behavioural contexts that vocalisations are produced in remains an important step towards understanding the functional relevance of specific call types in a given species’ vocal repertoire. In this study we investigated whether seasonal differences and the presence or absence of male and female conspecifics influence the production of male giant panda vocal signals. To this end, captive male giant pandas were observed during and outside of the breeding season in three social contexts: only male conspecific neighbours, only female conspecific neighbours, and a context with no neighbours. We found that males were more likely to bleat, chirp, honk and moan during the breeding season, and showed a tendency to growl more outside of the reproductive period. The contextual analysis revealed that bleats were more likely to be produced by males when opposite-sexed conspecifics are in close attendance during the breeding season. Conversely, males were more likely to chirp when neighboured by males than females or no neighbours. In addition, males were more likely to honk in the absence of neighbouring conspecifics during the breeding season, raising the possibility that these calls function to signal location and gain the attention of potential mates. Moans were produced more often when male giant pandas had male than female neighbours during the breeding season, which may reflect mild aggression towards these same-sexed rivals, whereas the production of barks and growls did not vary according to season or the sex of conspecific neighbours. Our findings underscore the importance of male giant panda bleats for coordinating reproduction and promoting contact with potential mating partners in this non-gregarious species, and yield fresh insights into the function of male honks that warrant further investigation. They also provide a basis for comparison with free-ranging giant panda vocal behaviour that could potentially inform conservation efforts.
    • Male European badger churrs: Insights into call function and motivational basis

      Charlton, Benjamin D.; Newman, Chris; Macdonald, David W.; Buesching, Christina D. (2020)
      Determining the contexts of emission and information content of vocal signals can yield insights into the function of different call types, and remains an important step towards understanding the diversification of mammalian vocal repertoires. In this study, we used infra-red video cameras and remote audio recorders to document seasonal and contextual variation in male European badger (Meles meles) churr production over a 24-month period, and acoustic analysis based on source-filter theory to examine whether churr acoustic structure varies according to the caller’s arousal state and identity….
    • Phenotypic plasticity in the timing of reproduction in Andean bears

      Appleton, R. D.; Van Horn, Russell C.; Noyce, K. V.; Spady, T. J.; Swaisgood, Ronald R.; Arcese, P. (2018)
      Many factors influence whether mammals reproduce seasonally or continuously but disentangling them can be challenging in free‐living species that are hard to observe. We described the seasonality of reproduction in Andean bears (Tremarctos ornatus) in NW Peru (6°26′S, 79°33′W) to test for phenotypic plasticity in response to extrinsic cues.
    • Reproductive performance parameters in a large population of game-ranched white rhinoceroses (Ceratotherium simum simum)

      Ververs, Cyrillus; Langhout, Martine van Zijll; Hostens, Miel; Otto, Michelle; Govaere, Jan; Durrant, Barbara S.; Soom, Ann Van (2017)
      The population of free-roaming white rhinoceroses (Ceratotherium simum) is under serious threat. Captive breeding of this species is therefore becoming more important, but this is challenging and often not successful. Obtaining reproductive reference values is a crucial aspect of improving these breeding results. In this study performed between 2008 and 2016, reproductive performance was analysed in 1,354 animals kept in a 8000 hectares game-ranched environment. Descriptive statistics of this captive population showed an average annual herd growth (%) of 7 .0±0.1 (min -9 –max 15). Average calving rates were calculated as an annual calving rate of 20% and biennial calving rate of 37% adult females calving per year. Females had a median age of 83.2 months at first calving (IQR 72.9–110.7) and inter-calving intervals of 29.2 (IQR 24.6–34.8) months. Furthermore, translocations of animals did not interfere with reproductive success in terms of inter-calving periods or age at first calving. Multivariate models showed a clear seasonal calving pattern with a significant increase of the number of calvings during December–April when compared to April–December. Our results did not show any significant skewed progeny sex ratios. Weather observations showed no significant influence of rain or season on sex ratios of the calves.
    • Reproductive techniques for ovarian monitoring and control in amphibians

      Calatayud, Natalie E.; Chai, Norin; Gardner, Nicole R.; Curtis, Michelle J.; Stoops, Monica A. (2019)
      Ovarian control and monitoring in amphibians require a multi-faceted approach. There are several applications that can successfully induce reproductive behaviors and the acquisition of gametes and embryos for physiological or molecular research. Amphibians contribute to one-quarter to one-third of vertebrate research, and of interest in this context is their contribution to the scientific community's knowledge of reproductive processes and embryological development. However, most of this knowledge is derived from a small number of species. In recent times, the decimation of amphibians across the globe has required increasing intervention by conservationists. The captive recovery and assurance colonies that continue to emerge in response to the extinction risk make existing research and clinical applications invaluable to the survival and reproduction of amphibians held under human care. The success of any captive population is founded on its health and reproduction and the ability to develop viable offspring that carry forward the most diverse genetic representation of their species. For researchers and veterinarians, the ability to monitor and control ovarian development and health is, therefore, imperative. The focus of this article is to highlight the different assisted reproductive techniques that can be used to monitor and, where appropriate or necessary, control ovarian function in amphibians. Ideally, any reproductive and health issues should be reduced through proper captive husbandry, but, as with any animal, issues of health and reproductive pathologies are inevitable. Non-invasive techniques include behavioral assessments, visual inspection and palpation and morphometric measurements for the calculation of body condition indices and ultrasound. Invasive techniques include hormonal injections, blood sampling, and surgery. Ovarian control can be exercised in a number of ways depending on the application required and species of interest.
    • Signalling behaviour is influenced by transient social context in a spontaneously ovulating mammal

      Owen, Megan A.; Swaisgood, Ronald R.; Zhou, Xiaoping; Blumstein, Daniel T. (2016)
      ...Using female giant pandas at the Wolong Breeding Centre in Sichuan, China, we explored the interaction between social context and reproductive status on signalling and maintenance behaviours. To do so, we used linear mixed models and an information-theoretic approach to assess the temporal relationship between signalling behaviours and the timing of first mating....
    • Stereotypic behaviour predicts reproductive performance and litter sex ratio in giant pandas

      Martin, Meghan S.; Owen, Megan A.; Wintle, Nathan J. P.; Zhang, Guiquan; Zhang, Hemin; Swaisgood, Ronald R. (2020)
      Breeding and welfare problems confront many conservation breeding programs. Stereotypies—repetitive, unvarying, functionless behaviours —are common abnormal behaviours that often arise in suboptimal conditions. While the role of stereotypies in welfare assessment is well studied, few investigations address the relationship between stereotypic behaviour and reproduction. We examined the correlation between stereotypic behaviour and reproductive performance in 101 giant pandas (Ailuropoda melanoleuca). High stereotyping males copulated more and produced more cubs, suggesting that highly sexually motivated males were prone to stereotypy but also had high reproductive competence. Female stereotypies were negatively associated with all reproductive measures closely tied to behavioural competence: high stereotyping females were less likely to copulate, less likely to mother-rear cubs, and—probably a result of poor maternal care—had lower cub survival. However, females that exhibited stereotypies were more likely to produce a cub, suggesting stereotypies are tied to behavioural but not physiological competence. High stereotyping female pandas also displayed strong and consistent bias toward production of female offspring while paternal relationship to sex allocation was the reverse. These results are consistent with stress-mediated sex allocation theory. Our findings raise concern about differential reproductive success among high and low stereotyping pandas, and possible genetic adaptation to captivity.
    • The acoustic structure of male giant panda bleats varies according to intersexual context

      Charlton, Benjamin D.; Keating, Jennifer L.; Rengui, Li; Huang, Yan; Swaisgood, Ronald R. (2015)
      ...These results show that acoustic features of male giant panda bleats have the potential to signal the caller's motivational state, and suggest that males increase the rate of fundamental frequency modulation in bleats when they are alone to maximally broadcast their quality and promote close-range contact with receptive females during the breeding season...
    • The influence of social context on animal behavior: Implications for conservation

      Owen, Megan A. (University of California, Los Angeles.Los Angeles, 2014)
      The pervasive perturbation of natural systems by human activities has rapidly changed the social context of many free-ranging animals, potentially reducing the efficiency of reproductive strategies, as well as the effective population size (Ne). Behavioral flexibility can be beneficial to species confronted with rapid contextual change, and the range of flexibility may ultimately influence whether a species can buy the time needed to respond adaptively to change. From the perspective of conservation management, an understanding of species' behavioral flexibility may improve predictions regarding the effects of rapid environmental change on populations, and facilitate the application of behavioral knowledge to conservation management. Fundamentally, an animal's decision-making processes are responsible for generating flexible behavioral responses, thus the lability of mechanisms underpinning decision-making influences the flexibility of behavioral responses. Here I evaluate the study of animal decision-making across scientific disciplines. I critically assess the use of animal decision-making in conservation and suggest ways in which decision theory could enhance conservation strategies. My empirical research is focused on the influence of social context on behavioral flexibility in the endangered giant panda (Ailuropoda melanoleuca). The panda is a compelling species in which to study behavioral flexibility in the conservation context, because they are solitary, and females are seasonally-monoestrus and ovulate spontaneously. While energetic constraints play a prominent role in reproductive strategies, little is known regarding their mating system or the plasticity of reproductive behavior. Pandas are behaviorally expressive, using multiple modes of signaling during courtship, however, a holistic understanding of multimodal signaling in the species is lacking. Further, although populations are depleted throughout most of their range, the influence of social context on behavior and communication has not been described. Here we show that female signaling effort is generally lower in the exclusive presence of other females, suggesting that females can modify their behavioural efforts during the pre-ovulatory period according to the prevailing social context. We also found that multimodal signaling during social interactions did not consistently evoke an immediate, discrete response from receivers. Together these findings suggest that giant pandas demonstrate a limited degree of flexible behavioral responses dependent upon the prevailing social context.
    • Vocal behaviour predicts mating success in giant pandas

      Charlton, Benjamin D.; Martin-Wintle, Meghan S.; Owen, Megan A.; Zhang, Hemin; Swaisgood, Ronald R. (2018)
      Surprisingly little is known about how mammal vocal signals are used to achieve behavioural synchrony in the lead up to copulation. The ability to signal short-term fluctuations in arousal levels and behavioural intention is likely to be particularly important for synchronizing mating behaviour in asocial species, which must overcome their natural avoidance and aggressive tendencies to mate. Here, we examined vocal behaviour during breeding encounters in captive giant pandas (Ailuropoda melanoleuca) to gain a greater understanding of how close-range vocal signalling mediates reproduction in this asocial, and conservation-dependent species. Our results revealed that the occurrence of different giant panda vocalizations and acoustic variation within these calls is predictive of successful encounters leading to copulation, as opposed to unsuccessful encounters that do not. In addition, key differences were detected between vocalizations produced during and just prior to copulation. These findings illustrate that vocal exchanges are crucial for achieving behavioural synchrony and signalling intention to mate in giant pandas, and could also provide a valuable tool for breeding programmes, helping conservation managers to assess the likelihood of breeding introductions leading to copulation or potentially injurious failure.