Design and test of novel scent enrichments to enhance breeding of zoo-housed lemurs.

Background: Zoos use environmental enrichments, including scents, which may have applications to improve breeding success for taxa, such as lemurs, which rely heavily on olfactory communication. We aimed to develop novel, biologically-relevant scent enrichments to trigger mating behaviours of zoo-housed lemur species, which are critically endangered in the wild and show a low success rate in captive breeding programmes. Methods: We examined anogenital odour secretions, released by female gentle ( Hapalemur alaotrensis) and ruffed ( Varecia variegata) lemurs, using solid-phase microextraction and gas chromatography-mass spectrometry techniques. We identified the key compounds distinguishing the volatile chemical profile of female lemurs during the breeding season and used them to develop species-specific scent enrichments. We then tested the scent enrichments, made up of synthesized mixtures conveying information about female lemur fertility, on unsuccessful breeding pairs of lemurs hosted in European zoos. We evaluated the effects of the newly designed scent enrichments on their target species by combining behavioural observations with faecal endocrinology. Results: We identified and reproduced fertility-specific signals associated with female scents. These scent mixtures triggered male sexual behaviours, including mating, during and after the enrichment condition. We also found effects on faecal testosterone levels, with increased levels after the enrichment condition albeit not statistically significant. Conclusions: Our findings suggest that biologically-relevant scent enrichments may trigger natural species-specific behaviours, with potential implications for conservation breeding of zoo-based endangered lemur species, and highlight that combining more assessment methods may assist with evaluating the impact of environmental enrichments.

The Scent Enriched Primate.

Zoos worldwide play an important role in both in situ and ex situ conservation via efforts such as providing breeding programmes and reintroductions into the wild. Zoo populations are crucial as a buffer against extinction. However, a mismatch between the wild and zoo environments can lead to psychological as well as physiological health issues, such as stress, boredom, diabetes, and obesity. These problems, in turn, can impact the reproductive success of individuals. Consequently, some primate species have reduced breeding success when housed in zoos compared to their wild counterparts. To prevent the onset of behavioural, physiological, and cognitive negative effects and to continually improve the welfare of their animals, zoos widely implement different types of environmental enrichment. There are many forms enrichment can take, such as feeding, puzzles and training, but sensory enrichments, including implementing the use of scents, are currently understudied. Scent enrichments are less utilized despite multiple research studies showing that they may have positive effects on welfare for zoo-housed animal species, including non-human primates. Despite being traditionally considered to be microsmatic, various lines of evidence suggest that olfaction plays a larger role in primates than previously thought. This review therefore focuses on scent-based enrichment and the specifics of captive primates.

Sexual Dimorphism in Crowned Lemur Scent-Marking.

Primates are traditionally considered to have a poor sense of smell. However, olfaction is important for non-human primates as demonstrated by conspicuous scent-marking behaviours in lemurs. We studied two pairs (n = 4) of crowned lemurs (Eulemur coronatus) housed at Colchester and Twycross zoos (UK) by combining behavioural observations and chemical analyses of scent-marks and glandular swabs. We recorded observations of olfactory behaviours for 201 h using instantaneous scan sampling. We investigated the volatile compounds of ano-genital odour secretions (n = 16) using solid-phase microextraction and gas chromatography-mass spectrometry. Males scent-marked most frequently, displaying ano-genital marking for allomarking, head marking for countermarking and wrist marking in specific areas of the enclosure. Females displayed ano-genital marking, predominantly on feeding devices. We detected a total of 38 volatile components in all male ano-genital scent-marks and 26 in all female samples of ano-genital odour secretions, including a series of esters, aldehydes, ketones, alcohols, terpenes, volatile fatty acids and hydrocarbons that have been identified in odour profiles of other primates. In conclusion, we found sexual dimorphism in crowned lemur scent-marking. Male head and wrist marking behaviours might play defensive territorial functions, while ano-genital marking would be related to socio-sexual communication as chemical mate-guarding. Female ano-genital marking might be involved in resource defense.

Effects of scent enrichment on behavioral and physiological indicators of stress in zoo primates.

Captive breeding is vital for primate conservation, with modern zoos serving a crucial role in breeding populations of threatened species and educating the general public. However, captive populations can experience welfare issues that may also undermine their reproductive success. To enhance the wellbeing of endangered zoo primates, we conducted a study to assess the effects of a new scent enrichment program on captive red-ruffed lemurs (Varecia rubra), black howler monkeys (Alouatta caraya), siamangs (Symphalangus syndactylus), lar gibbons (Hylobates lar) and orangutans (Pongo pygmaeus pygmaeus). We combined behavioral observations and fecal endocrinology analyses to evaluate the effects of a series of essential oils (benzoin, lavender, lemongrass) on five captive troops (N = 19) housed at Dudley Zoo & Castle and Twycross Zoo (UK). We recorded observations of natural species-specific and abnormal stress-related behaviors for 480 h using instantaneous scan sampling. We collected 189 fecal samples and measured the fecal cortisol concentrations using radioimmunoassay. We found a significant effect of the scent enrichment on behaviors, with red-ruffed lemurs and black howler monkeys reducing their social interactions, as well as red-ruffed lemurs and lar gibbons decreasing their stress-related behaviors after they were exposed to the series of essential oils. We also found that red-ruffed lemurs displayed a significant increase in fecal glucocorticoids following exposure to essential oils. Our contradictory findings suggest that the effects of this series of essential oils may change depending on the species-specific social lives and olfactory repertoires of primates. In conclusion, we cannot recommend using these essential oils widely with zoo primates without additional evaluation.

The effects of a zoo environment on free-living, native small mammal species.

One of the main threats to native species conservation is urbanisation. It is causing changes to natural habitats and species composition. Urban green spaces have shown to have conservation value for native species by providing safe spaces in urban areas. They typically contain a variety of habitats and plant species which is correlated with greater abundance and diversity of small mammal species. Zoos are a vital resource for animal conservation and, in some instances, could be considered as an urban green space for native species conservation. Their unique environment provides free-living, native species an abundance of resources including food and shelter. This project involved the live trapping of free-living small mammal species (<40 g) between enclosures in Dudley Zoological Gardens to study the effects of the zoo environment. There were no significant differences found between the total number of captures and trap proximity to enclosures. There was a significant difference in total captures found between different enclosure trapping areas. Generalized linear mixed models were fitted to the data and there were significant relationships between abundance and both habitat type and enclosure species. Habitats associated with semi-natural woodland had the greatest diversity and total captures of small mammals. Total captures were lower in trapping areas that were associated with predatory species. Similar to research on green spaces, habitat was an important factor determining abundance, but predator enclosures were a factor unique to zoos. This study illustrates the potential of zoos as an urban green space and for the study of small mammals.