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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., Competing Interests: No competing interests were disclosed., (Copyright: © 2024 Elwell E et al.)

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., (© 2021 The Authors. American Journal of Primatology Published by Wiley Periodicals LLC.)

Female primates signal impending ovulation with a suite of sexual signals. Studies of these signals have focussed on visual, and to a lesser extent, acoustic signals, neglecting olfactory signals. We aimed to investigate the information content of female olfactory signals in captive olive baboons (Papio anubis) and relate these to the female fertile period. We studied eight adult females living in four groups at the CNRS Station de Primatologie, Rousset-sur-Arc, France. We used vaginal cytology to detect ovulation. We investigated the volatile component of odour signals using solid-phase microextraction and gas chromatography-mass spectrometry. We found a total of 74 volatile compounds, of which we tentatively identified 25, including several ketones, alcohols, aldehydes, terpenes, volatile fatty acids and hydrocarbons that have been identified in odour profiles of other primates. Our results show that vaginal odour intensity differs with sexual cycle stage suggesting that odour might play a role in signalling female baboon fertility. We found differences in vaginal odour between females living in all-female and in mixed sex groups but we could not distinguish the effects of group composition, female age and identity. This study of olfactory signalling improves our understanding of how female primates advertise their sexual receptivity.

We have developed an effective methodology for sampling and analysis of odor signals, by using headspace solid-phase microextraction coupled with gas chromatography-mass spectrometry, to understand how they may be used in animal communication. This technique allows the semi-quantitative analysis of the volatile components of odor secretions by enabling the separation and tentative identification of the components in the sample, followed by the analysis of peak area ratios to look for trends that could signify compounds that may be involved in signaling. The key strengths of this current approach are the range of sample types that can be analyzed; the lack of need for any complex sample preparation or extractions; the ability to separate and analyze the components of a mixture; the identification of the components detected; and the capability to provide semi-quantitative and potentially quantitative information on the components detected. The main limitation to the methodology relates to the samples themselves. Since the components of specific interest are volatile, and these could easily be lost, or their concentrations altered, it is important that the samples are stored and transported appropriately after their collection. This also means that sample storage and transport conditions are relatively costly. This method can be applied to a variety of samples (including urine, feces, hair and scent-gland odor secretions). These odors consist of complex mixtures, occurring in a range of matrices, and thus necessitate the use of techniques to separate the individual components and extract the compounds of biological interest.

Primate chemical communication remains underappreciated, as primates are considered to rely on other sensory modalities. However, various lines of evidence suggest that olfaction plays an important role in primate societies, including the conspicuous scent-marking behavior of many strepsirrhines and callitrichines. Although lemurs typically show scent-marking, little is known about this behavior in red-ruffed lemurs (Varecia variegata rubra). We combined behavioral observations and semiochemistry analyses to improve our understanding of scent-marking in two captive troops housed at Dudley and Twycross zoos (UK). We collected olfactory behavioral observations by focusing on two family troops (N = 7) for 132 hr. We investigated the volatile compounds of ano-genital scent-marks using solid-phase microextraction and gas chromatography-mass spectrometry and compared volatile chemical profiles with features of the signaller. Males scent-marked most frequently and predominantly in specific meaningful areas of the enclosure, while within females the occurrence of scent-marking was related to their age. We found behavioral sexual dimorphism, with male predominantly depositing secretions via neck and mandible glands and females via ano-genital glands. We identified a total of 32 volatile components of ano-genital gland secretion, including compounds that have already been found in other mammals as sex pheromones and cues to fitness, in ano-genital scent-marks spontaneously left on filter paper by adult females. Our findings suggest that red-ruffed lemurs might use scent-marking to convey information about sex and female age, with male neck-marking behavior playing defensive territorial functions and ano-genital marking related to socio-sexual communication., (© 2019 Wiley Periodicals, Inc.)

Mandrills are one of the few Old World primates to show scent-marking. We combined ethological and chemical approaches to improve our understanding of this behavior in 3 zoo-managed groups. We observed the olfactory behavior performed by adults and adolescents (N = 39) for 775h. We investigated the volatile components of sternal scent-marks using gas chromatography-mass spectrometry and compared volatile profiles with traits of the signaler. Males marked more than females and within each sex the frequency of scent-marking was related to age and dominance status, but alpha males scent-marked most frequently and particularly in specific areas at the enclosure boundaries. We identified a total of 77 volatile components of sternal gland secretion, including compounds functioning as male sex pheromones in other mammals, in scent-marks spontaneously released on filter paper by 27 male and 18 female mandrills. We confirmed our previous findings that chemical profiles contain information including sex, male age and rank, and we also found that odor may encode information about group membership in mandrills. Our results support the hypotheses that scent-marking signals the status of the dominant male as well as playing territorial functions but also suggest that it is part of sociosexual communication., (© The Author 2015. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.)

The major histocompatibility complex (MHC) is an extraordinarily diverse cluster of genes that play a key role in the immune system. MHC gene products are also found in various body secretions, leading to the suggestion that MHC genotypes are linked to unique individual odourtypes that animals use to assess the suitability of other individuals as potential mates or social partners. We investigated the relationship between chemical odour profiles and genotype in a large, naturally reproducing population of mandrills, using gas chromatography-mass spectrometry and MHC genotyping. Odour profiles were not linked to the possession of particular MHC supertypes. Sex influenced some measures of odour diversity and dominance rank influenced some measures of odour diversity in males, but not in females. Odour similarity was strongly related to similarity at the MHC, and, in some cases, to pedigree relatedness. Our results suggest that odour provides both a cue of individual genetic quality and information against which the receiver can compare its own genotype to assess genetic similarity. These findings provide a potential mechanism underlying mate choice for genetic diversity and MHC similarity as well as kin selection.

Scents play a key role in mediating reproductive interactions in many vertebrates including mammals. Nowadays, several studies indicate that humans seem to use remarkably olfactory communication and are even able to produce and perceive pheromones. Furthermore, over the past several years, it became increasingly clear that pheromone-like chemical signals probably play a role in offspring identification and mother recognition. Recently developed technical procedures (solid-phase microextraction and dynamic headspace extraction) now allow investigators to characterize volatile compounds with high reliability. We analyzed the volatile compounds in sweat patch samples collected from the para-axillary and nipple-areola regions of women during pregnancy and after childbirth. We hypothesized that, at the time of birth and during the first weeks of life, the distinctive olfactory pattern of the para-axillary area is probably useful to newborn babies for recognizing and distinguishing their own mother, whereas the characteristic pattern of the nipple-areola region is probably useful as a guide to nourishment., (Copyright © 2010 Elsevier Inc. All rights reserved.)