Sex differences in scent‐marking in captive red‐ruffed lemurs

Abstract

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 neckmarking behavior playing defensive territorial functions and ano-genital marking related to socio-sexual communication. K E Y W O R D S communication, gas chromatography-mass spectrometry, olfaction, signaling, Varecia variegata rubra

Olfactory signals and fertility in olive baboons

“…Among the acids (2-methyl propanoic acid, butyric acid, 2-methyl hexadecanoic acid, and benzoic acid), we found the compound butyric acid that is one of the five aliphatic acids, named “copulins”, which were also found in women’s vaginal secretions and considered to contribute to making these vaginal secretions attractive to males 89 . Likewise, methoxy-phenyl-oxime was identified in human axillary sweat 90 , and reported as a minor constituent of essential oils and aromatic extracts 91 ; conversely, the other compound which we found with highest abundance and most change from sample to sample, p -cresol, has previously been identified in female scent-marks by red-ruffed lemurs 84 and capuchin monkeys 92 as well as a component of the female sex pheromone in the horse ( Equus caballus ). Additionally, the compounds benzoic acid, hexanal and 1-Octen-3-ol are encountered in odour secretions used to scent-mark by several non-primate mammals (e.g., lions ( Panthera leo ), African wild dogs ( Lycaon pictus ), gray wolves ( Canis lupus ), house mice ( Mus musculus ), red foxes ( Vulpes vulpes )) (reviewed in 93 ) and primates (e.g., aye-ayes ( Daubentonia madagascariensis ) 94 , red-ruffed lemurs 84 , ring-tailed lemurs 43 , Coquerel’s sifakas 83 , common marmosets 95 ) (see Table 2 for details).…”

“…Likewise, methoxy-phenyl-oxime was identified in human axillary sweat 90 , and reported as a minor constituent of essential oils and aromatic extracts 91 ; conversely, the other compound which we found with highest abundance and most change from sample to sample, p -cresol, has previously been identified in female scent-marks by red-ruffed lemurs 84 and capuchin monkeys 92 as well as a component of the female sex pheromone in the horse ( Equus caballus ). Additionally, the compounds benzoic acid, hexanal and 1-Octen-3-ol are encountered in odour secretions used to scent-mark by several non-primate mammals (e.g., lions ( Panthera leo ), African wild dogs ( Lycaon pictus ), gray wolves ( Canis lupus ), house mice ( Mus musculus ), red foxes ( Vulpes vulpes )) (reviewed in 93 ) and primates (e.g., aye-ayes ( Daubentonia madagascariensis ) 94 , red-ruffed lemurs 84 , ring-tailed lemurs 43 , Coquerel’s sifakas 83 , common marmosets 95 ) (see Table 2 for details). The compound benzaldehyde is considered a crucial putative semiochemical occurring at all ancestral nodes leading to both urine and glandular markers in many strepsirrhine species 96 ; this compound has also been found in scent gland secretions released by ayes-ayes 94 , red-ruffed lemurs 84 , common marmosets 95 , capuchin monkeys 92 , emperor tamarins 97 , Weddell’s saddleback tamarins 97 , owl monkeys (where the presence of this compound has also been validated with internal standards) 57 and mandrills 39 , 40 , and acts as a sex pheromone in other mammals and as an alarm pheromone in invertebrates such as stingless bees ( Tetragonisca angustula ) (reviewed in 73 ).…”

“…Additionally, the compounds benzoic acid, hexanal and 1-Octen-3-ol are encountered in odour secretions used to scent-mark by several non-primate mammals (e.g., lions ( Panthera leo ), African wild dogs ( Lycaon pictus ), gray wolves ( Canis lupus ), house mice ( Mus musculus ), red foxes ( Vulpes vulpes )) (reviewed in 93 ) and primates (e.g., aye-ayes ( Daubentonia madagascariensis ) 94 , red-ruffed lemurs 84 , ring-tailed lemurs 43 , Coquerel’s sifakas 83 , common marmosets 95 ) (see Table 2 for details). The compound benzaldehyde is considered a crucial putative semiochemical occurring at all ancestral nodes leading to both urine and glandular markers in many strepsirrhine species 96 ; this compound has also been found in scent gland secretions released by ayes-ayes 94 , red-ruffed lemurs 84 , common marmosets 95 , capuchin monkeys 92 , emperor tamarins 97 , Weddell’s saddleback tamarins 97 , owl monkeys (where the presence of this compound has also been validated with internal standards) 57 and mandrills 39 , 40 , and acts as a sex pheromone in other mammals and as an alarm pheromone in invertebrates such as stingless bees ( Tetragonisca angustula ) (reviewed in 73 ). Interestingly, methyl ketones, which are found as putative semiochemicals in aye-ayes 94 and red-ruffed lemurs 84 , dominate females’ skin pheromone blend in garter snakes ( Thamnophis sirtalis parietalis ), and their presence and relative abundance are used by males to choose female mates with potential for production of more offspring per litter 98 .…”

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

“…Interestingly, we found that scent enrichment exerted both behavioural and physiological effects on both red-ruffed lemurs and Lar gibbon. While the use of chemical communication and olfactory signals in lemurs has long been established [51][52][53], apes are commonly considered microsmatic. However, accumulating evidence seems to suggest that apes may also rely on olfactory signals and chemical communication.…”

“…Although primates have traditionally been considered to be “microsmatic” with a simultaneous amplified emphasis on vision (Dominy & Lucas, 2001; Fornalé et al, 2012; Gerald, 2003), several studies suggest that chemical communication is important also for primate species (reviewed by Drea, 2020). Particularly, it is established that some species rely heavily on olfaction in addition to vision and auditory senses; for instance, this is the case of several lemurs (Gould & Overdorff, 2002; Janda et al, 2019; Scordato & Drea, 2007) and squirrel monkeys (Laska et al, 2000). This would explain the significant impact of our scent enrichment on red-ruffed lemurs, rather than the other study species for which no such response was observed, as lemurs have retained a greater olfactory complexity than other lineages such as monkeys and apes.…”