Behav Ecol Sociobiol (2015) 69:2019–2034 DOI 10.1007/s00265-015-2013-y ORIGINAL ARTICLE Rhesus macaques (Macaca mulatta) recognize group membership via olfactory cues alone Stefanie Henkel 1,2 & Angelina Ruiz Lambides1,3,4 & Anne Berger5 & Ruth Thomsen1,6,7 & Anja Widdig1,3 Received: 9 April 2015 /Revised: 18 September 2015 /Accepted: 21 September 2015 /Published online: 31 October 2015 # Springer-Verlag Berlin Heidelberg 2015 Abstract The ability to distinguish group members from con- paradigm to investigate whether rhesus macaques (Macaca specifics living in other groups is crucial for gregarious spe- mulatta) can discriminate between body odors of female cies. Olfaction is known to play a major role in group recog- group members and females from different social groups. nition and territorial defense in a wide range of mammalian We conducted the study on the research island Cayo Santiago, taxa. Although primates have been typically regarded as Puerto Rico, in the non-mating season and controlled for kin- microsmatic (having a poor sense of smell), increasing evi- ship and familiarity using extensive pedigree and demograph- dence suggests that olfaction may play a greater role in pri- ic data. Our results indicate that both males and females in- mates’ social life than previously assumed. In this study, we spect out-group odors significantly longer than in-group carried out behavioral bioassays using a signaler-receiver odors. Males licked odors more often than females, and older animals licked more often than younger ones. Furthermore, individuals tended to place their nose longer towards odors Communicated by E. Huchard when the odor donor’s group rank was higher than the rank of Electronic supplementary material The online version of this article their own group. Reuse of odor samples decreased odor inten- (doi:10.1007/s00265-015-2013-y) contains supplementary material, sity (rated by human experimenters) during the course of a which is available to authorized users. given test day and with longer exposure to ambient air; how- ever, the reuse of odor samples did not significantly influence * Stefanie Henkel the response behaviors. Our findings uncover key roles of [email protected]; [email protected] olfactory communication in a species not possessing distinct scent glands and thus shed light into the evolution of primate 1 Behavioral Ecology Research Group, Institute of Biology, Faculty of olfactory communication. Bioscience, Pharmacy and Psychology, University of Leipzig, Talstrasse 33, 04103 Leipzig, Germany . 2 Keywords Olfactory communication Rhesus macaques Department of Developmental and Comparative Psychology, Max Bioassay . Group recognition . Individual recognition . Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany Familiarity 3 Junior Research Group of Primate Kin Selection, Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany Introduction 4 Caribbean Primate Research Center, University of Puerto Rico, Medical Sciences Campus, Puerto Rico, USA For gregarious species, the ability to distinguish group mem- 5 Leibniz Institute for Zoo and Wildlife Research, Alfred-Kowalke-Str. bers (in-group individuals) from conspecifics living in other 17, 10315 Berlin, Germany groups (out-group individuals) is of crucial importance as it 6 Department of Anthropology, University College London, Gower allows individuals of the same group to protect resources such Street,LondonWC1E6BT,UK as food, mating partners, or sleeping sites against intruders 7 Department of Primatology, Max Planck Institute for Evolutionary while ensuring social cohesion within the group. In addition Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany to visual (domestic cattle, Coulon et al. 2010;Barbary 2020 Behav Ecol Sociobiol (2015) 69:2019–2034 macaques, Schell et al. 2011) and acoustic (elephants, with the processing of non-volatile odorants by the McComb et al. 2000; chimpanzees, Herbinger et al. 2009; vomeronasal organ (Charpentier et al. 2013). Furthermore, horses, Lemasson et al. 2009; dolphins, Quick and Janik western lowland gorillas (Gorilla gorilla gorilla) are able to 2012) cues, olfaction plays a major role in group recognition discriminate between different odors such as almond and and territorial defense in a wide range of taxa (reviewed, for vanilla (Hepper and Wells 2012) and produce individual mammals, in Tang Halpin 1986). For example, black-tailed body odors which can be identified by human raters deer (Odocoileus hemionus columbianus, Müller-Schwarze (Hepper and Wells 2010). 1971), African dwarf mongoose (Helogale undulata rufula, In order to fully assess the importance of olfactory commu- Rasa 1973), and Mongolian gerbils (Meriones unguiculatus, nication in the primate order and to shed light on its evolution, Tang Halpin 1976) treat familiar individuals and strangers it is essential to consider catarrhine species without distinct differently, discriminating between them using olfactory cues. scent glands and scent-marking behavior as well. There is Domestic dogs (Dunbar and Carmichael 1981), horses (Equus very limited information on olfactory behavior in species caballus, Péron et al. 2014), and Columbian ground squirrels which lack these features (chimpanzees, Pan troglodytes, (Spermophilus columbianus, Harris and Murie 1982)alsodis- Mitani and Watts 2005; Herbinger et al. 2009; chacma ba- criminate between in-group and out-group individuals, spend- boons, Papio hamadryas ursinus,Clarkeetal.2009). Rhesus ing more time investigating odors from unfamiliar conspe- macaques (Macaca mulatta) represent an ideal model species cifics as compared to odors from group or colony members. as they have been observed to use olfaction in a variety of In primates, however, the role of olfaction is far less under- contexts, although they do not seem to possess scent glands stood than in other mammalian species, most likely because and do not perform scent marking (Geissmann 1987). They primates were typically regarded as microsmatic, relying more inspect food via smelling and sniff various body parts includ- on visual and acoustic rather than on olfactory information. ing the head or anus of conspecifics, and males sniff females’ The olfactory bulbs and olfactory epithelia are proportionately genitals, especially during the mating season (SH, personal smaller in primates compared to most other mammals (Baron observation). Rhesus macaques on Cayo Santiago were re- et al. 1983; Smith and Bhatnagar 2004), and among primates, cently observed to exhibit exploratory behavior, including the ratio between total brain volume and olfactory bulb vol- smelling, towards the body of a dead and heavily injured ume decreases from strepsirrhines to anthropoids (Stephan monkey (Buhl et al. 2012), possibly to gain information about et al. 1970). Despite the anatomical evidence for a relative its individual identity or group membership. Furthermore, as reduction in olfactory structures during primate evolution, it rhesus macaques are considered to be a highly despotic spe- is currently debated whether this corresponds to a functional cies demonstrating high levels of intra- and intergroup ag- reduction in olfactory abilities of Old World monkeys. In fact, gression (Loy 1970; Boelkins and Wilson 1972; Flack and a growing body of evidence suggests that olfactory commu- de Waal 2004), they are ideal to study the mechanisms of nication may play a significant role in the regulation of a wide group recognition in primates. range of primate behaviors (Heymann 2006;Drea2015). While visual cues appear to be well suited for individual or Strepsirrhines and New World monkeys, in particular, appear group recognition during daytime (Pokorny and de Waal to have well-developed olfactory capabilities with odor cues 2009;Schelletal.2011), olfactory cues pertaining to group indicating reproductive state, dominance rank, individual membership are also available at night. Nocturnal primates are identity, and even genetic information which can be perceived known to rely heavily on their olfactory sense. Owl monkeys by the animals (e.g., cotton-top tamarins, Saguinus oedipus, (Aotus nancymaae), for example, are able to recognize sex, Ziegler et al. 1993; common marmosets, Callithrix jacchus, age, and family membership via olfactory cues (MacDonald Smith et al. 1997; ring-tailed lemurs, Lemur catta, Palagi and et al. 2008). Nocturnal activity including moving, vocalizing, Dapporto 2006; Scordato and Drea 2007; Charpentier et al. feeding, or even playing has also been described for several 2008; Charpentier et al. 2010). diurnal primate species (gelada baboons, Theropithecus In contrast, very little is known about the olfactory capa- gelada, Kawai and Iwamoto 1979; Japanese macaques, bilities of Old World monkeys and apes, although recent evi- Nishikawa and Mochida 2010; ring-tailed lemurs, Donati dence indicates that, in these taxa, chemical communication et al. 2013; Guizhou snub-nosed monkeys, Rhinopithecus plays an important role as well. Most evidence until now has brelichi, Tan et al. 2013; chimpanzees, Zamma 2014;Krief come from species which perform classical scent marking et al. 2014) including rhesus macaques (Vessey 1973). Thus, and/or have specific glands used for olfactory communication. olfactory signals and body odor may play an important role Mandrills (Mandrillus sphinx), for example, signal both vari- when it comes to territorial defense