Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone

Henkel, Stefanie; Ruíz-Lambides, Angelina; Berger, Anne; Thomsen, Ruth; Widdig, Anja

doi:10.1007/s00265-015-2013-y

Cited by 25 publications

(23 citation statements)

References 109 publications

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“…Although differences in the overall similarity of axillary odorants were not very pronounced, differences in chemical composition persisted even when close relatedness ( r ≥ 0.25) was controlled. It should also be noted that these group differences are perceived by unrelated conspecifics, as previously shown in a bioassay study by Henkel et al ( 2015 ) in the same study population. The compounds distinguishing the different social groups best comprised three steroids, suggesting that hormonal differences arising from group-specific behavior and rank differences may be at the base of the detected differences in axillary secretions.…”

Section: Discussionsupporting

confidence: 71%

“…As in many other OWM, visual and acoustic communication play an important role in mediating rhesus social interactions (e.g., Higham et al 2013 ; Pfefferle et al 2015 ), while the role of olfactory communication is little explored. Yet, behavioral evidence indicates that rhesus macaques discriminate between social groups via olfactory cues alone (Henkel et al 2015 ), and we can expect rhesus body odors to relate also to other relevant social or individual attributes, either as by-products of physiological processes and/or as signals evolved for communication. Therefore, we collected axillary secretions of semifree-ranging rhesus macaques from the island of Cayo Santiago (Puerto Rico) and combined individual chemical profiles obtained by GC–MS analysis with demographic and genetic data.…”

Section: Introductionmentioning

confidence: 99%

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Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques

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Kücklich

Thomsen

et al. 2018

Behav Ecol Sociobiol

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Scents play an important role in the life of most terrestrial mammals and may transmit valuable information about conspecifics. Olfaction was long considered of low importance in Old World monkeys due to their relative reduction of olfactory structures and low incidence of scent-marking behavior but has been increasingly recognized for mediating social relationships in recent years. Yet, studies investigating the composition of their chemical cues remain scarce. In the present study, we analyzed the potential information content of chemicals present on the skin of rhesus macaques (Macaca mulatta). We collected axillary secretions from 60 animals of the semifree-ranging population on Cayo Santiago (Puerto Rico, USA) with precleaned cotton swabs from which the secretions were subsequently extracted and analyzed by gas chromatography–mass spectrometry. Rhesus macaque axillary odorants varied in their overall similarity and composition. This variation was attributable to differences in sex, group membership, and kinship and further appeared to reflect age and rank in parts of our sample. The compounds most strongly associated with this variation primarily comprised larger molecular weight aldehydes and steroids. Such compounds are considered to be perceivable by the primate olfactory system through close-range interactions or through breakdown into smaller molecules by bacterial fermentation. Overall, our results provide additional evidence that odors of Old World monkeys reflect a wealth of potential information about their carrier, which provides the basis for chemical communication via body odors; however, its use by conspecifics needs to be confirmed in bioassays.Significance statementOne prerequisite for olfactory communication is the presence of systematic variation in animal odors that is related to attributes such as age, sex, or kinship. The composition of odors has been examined in numerous mammals but, with the exception of humans, remains poorly understood in Old World monkeys and apes, taxonomic groups in which most species do not show scent-marking behavior. In the present study, we show that the composition of axillary secretions of an Old World monkey, the rhesus macaque, reflects sex, group membership, relatedness, and possibly also age and rank. This variation thus provides a basis for olfactory communication in Old World monkeys.Electronic supplementary materialThe online version of this article (10.1007/s00265-018-2479-5) contains supplementary material, which is available to authorized users.

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Section: Discussionsupporting

confidence: 71%

Section: Introductionmentioning

confidence: 99%

Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques

Weiß

Kücklich

Thomsen

et al. 2018

Behav Ecol Sociobiol

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“…Based on this finding, we infer that vaginal acidity in the surveyed macaques could be maintained by a variety of bacteria such as Fastidiosipila , Murdochiella , Peptoniphilus and Dialister by producing acetic acid to lower pH environment and protect from invasive pathogens. The presence of fermentative bacteria in the macaque vagina could be conserved in NHPs but not humans as the volatile short chain fatty acids produced can be used as scents for communication, social interaction and other olfactory-driven behaviour 47 , which arguably is less important in humans. Alternatively, a shift towards high starch diets of human beings associated with modernisation is probably responsible for lactobacilli dominance through increased vaginal glycogen content, resulting in low pH conditions in their reproductive physiology 24 .…”

Section: Discussionmentioning

confidence: 99%

Diversity of macaque microbiota compared to the human counterparts

Chen

Yeoh

Hui

et al. 2018

Sci Rep

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Studies on the microbial communities in non-human primate hosts provide unique insights in both evolution and function of microbes related to human health and diseases. Using 16S rRNA gene amplicon profiling, we examined the oral, anal and vaginal microbiota in a group of non-captive rhesus macaques (N = 116) and compared the compositions with the healthy communities from Human Microbiome Project. The macaque microbiota was dominated by Bacteroidetes, Firmicutes and Proteobacteria; however, there were marked differences in phylotypes enriched across body sites indicative of strong niche specialization. Compared to human gut microbiota where Bacteroides predominately enriched, the surveyed macaque anal community exhibited increased abundance of Prevotella. In contrast to the conserved human vaginal microbiota extremely dominated by Lactobacillus, the macaque vaginal microbial composition was highly diverse while lactobacilli were rare. A constant decrease of the vaginal microbiota diversity was observed among macaque samples from juvenile, adult without tubectomy, and adult with tubectomy, with the most notable distinction being the enrichment of Halomonas in juvenile and Saccharofermentans in contracepted adults. Both macaque and human oral microbiota were colonized with three most common oral bacterial genera: Streptococcus, Haemophilus and Veillonella, and shared relatively conserved communities to each other. A number of bacteria related to human pathogens were consistently detected in macaques. The findings delineate the range of structure and diversity of microbial communities in a wild macaque population, and enable the application of macaque as an animal model for future characterization of microbes in transmission, genomics and function.

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“…Having more knowledge on the detection distances of these signals could enable field scientists to exclude visual cues and could enable us to extend the research to species and locations where experiments are not feasible. Studies on such sensory abilities, especially on olfactory detection fields, are surprisingly limited to date (but see 150,151,153,154,181,182 ) and would greatly strengthen the conclusions field-based science can draw.…”

Section: Discussionmentioning

confidence: 99%

What animals do not do or fail to find: A novel observational approach for studying cognition in the wild

Janmaat

2019

Evolutionary Anthropology

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To understand how our brain evolved and what it is for, we are in urgent need of knowledge about the cognitive skills of a large variety of animal species and individuals, and their relationships to rapidly disappearing social and ecological conditions. But how do we obtain this knowledge? Studying cognition in the wild is a challenge. Field researchers (and their study subjects) face many factors that can easily interfere with their variables of interest. Although field studies of cognition present unique challenges, they are still invaluable for understanding the evolutionary drivers of cognition. In this review, I discuss the advantages and urgency of field‐based studies on animal cognition and introduce a novel observational approach for field research that is guided by three questions: (a) what do animals fail to find?, (b) what do they not do?, and (c) what do they only do when certain conditions are met? My goal is to provide guidance to future field researchers examining primate cognition.

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Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone

Cited by 25 publications

References 109 publications

Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques

Chemical composition of axillary odorants reflects social and individual attributes in rhesus macaques

Diversity of macaque microbiota compared to the human counterparts

What animals do not do or fail to find: A novel observational approach for studying cognition in the wild

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