Primates (2007) 48:160–163 DOI 10.1007/s10329-006-0019-9
S H O R T C O M M U NI C A T I O N
Self-anointing behavior in free-ranging spider monkeys (Ateles geoffroyi) in Mexico Matthias Laska Æ Verena Bauer Æ Laura Teresa Hernandez Salazar
Received: 8 August 2006 / Accepted: 20 September 2006 / Published online: 14 November 2006 Ó Japan Monkey Centre and Springer 2006
Abstract During 250 h of observation, a total of 20 episodes of self-anointing, that is, the application of scent-bearing material onto the body, were recorded in a group of free-ranging Mexican spider monkeys (Ateles geoffroyi). The animals used the leaves of three species of plants (Brongniartia alamosana, Fabaceae; Cecropia obtusifolia, Cecropiaceae; and Apium graveolens, Umbelliferae) two of which have not been reported so far in this context in any New World primate species. The findings that only two males displayed self-anointing, that only the sternal and axillary regions of the body were rubbed with the mix of saliva and plant material, and a lack of correlation between the occurrence of self-anointing and time of day, season of the year, ambient temperature or humidity do not fit the hypothesis that this behavior functions in repelling insects and/or mitigating topical skin infections in this species. Rather, the data and the observation that the leaves of all three plant species spread an intensive and aromatic odor when crushed, support the hypothesis that self-anointing in A. geoffroyi may play a role in the context of social communication, possibly for signaling of social status or to increase sexual attractiveness.
M. Laska (&) V. Bauer Department of Medical Psychology, University of Munich Medical School, Goethestr. 31, 80336 Munich, Germany e-mail:
[email protected] L. T. H. Salazar Instituto de Neuro-Etologia, Universidad Veracruzana, Xalapa, Veracruz, Mexico
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Keywords Ateles geoffroyi Spider monkeys Self-anointing Fur rubbing Mexico Olfactory communication
Introduction A variety of mammalian species have been reported to rub on, or roll in, selected plants, arthropods, and other scent-bearing material. It has been proposed that this behavior, often referred to as self-anointing, fur rubbing, or scent rubbing, may serve functions as diverse as repelling insects and ectoparasites, providing topical skin treatment for wounds or fungal and bacterial infections, increasing sexual attractiveness, signaling social status, providing scent camouflage, deterring predators, producing an agreeable sensation on the skin, and inducing a psychotropic state (Gosling and McKay 1990; Rodriguez and Wrangham 1993; Weldon 2004; Carroll et al. 2005). In nonhuman primates, self-anointing with leaves and other parts of selected plant species or millipedes has been reported in capuchin monkeys (Cebus spp.; Baker 1996; Gilbert et al. 1998; Gilbert and Boysen 1999; Valderrama et al. 2000; DeJoseph et al. 2002; Weldon et al. 2003), owl monkeys (Aotus trivirgatus; Evans et al. 2003; Zito et al. 2003), spider monkeys (Ateles geoffroyi; Campbell 2000), and in lemurs (Eulemur macaco; Birkinshaw 1999). The present paper describes the first observation of self-anointing in free-ranging spider monkeys in Mexico with three species of plants, two of which have not yet been reported to be used in this context in any New World primate species.
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Methods
Results During 250 h of observation, a total of 20 episodes of self-anointing performed by two adult males (12 and 8 episodes, respectively) were recorded. The monkeys used the leaves of Brongniartia alamosana (Fabaceae; 6 episodes), Cecropia obtusifolia (Cecropiaceae; 6 episodes) and Apium graveolens (Umbelliferae; 8 episodes). The behavioral pattern usually involved biting into or chewing the leaves, then rubbing the mixture of saliva and plant material onto the axillary and sternal regions of the ventrum. In the majority of cases, the arm that did not hold the scent-bearing material was held up high or grabbed a branch above the animal. A bout of self-anointing lasted between 30 s and 2 min (69 ± 35 s, mean ± SD) and always involved only one plant species at a time. With only three exceptions, the episodes occurred on different days, and in the few cases of multiple episodes of self-anointing on a given day these were separated by at least 90 min. There was no indication that self-anointing by one animal induced the same behavior in a conspecific. No correlation between the occurrence of self-anointing and time of day, season of the year, ambient temperature or humidity was observed (Fig. 1).
Discussion Self-anointing has so far been reported in three genera of New World primates, Cebus, Aotus, and Ateles. In
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Between July and December 2005 research was conducted on a group of free-ranging spider monkeys (A. geoffroyi) at the Parque de Flora y Fauna Silvestre Tropical, located near Catemaco, Veracruz, Mexico. The forest is classified as neotropical rain forest with an average of 4,900 mm of rainfall per year. The group of spider monkeys consisted of three adult females, six adult males, and one female infant. The unusual group composition was due to the fact that these animals had been reintroduced to this region about one year prior to the start of the study and built a rather stable group rather than dispersing and attaching to existing local groups of spider monkeys. Episodes of self-anointing were recorded ad libitum, and information on the plant species used, the part of the body rubbed with the plant, the individual animal performing the behavior, time of day, and climatic conditions was recorded.
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Fig. 1 Mean rainfall (mm/month, open circles), mean temperature (°C, open squares), and occurrence of self-anointing (filled circles) during the six-month study period
capuchin monkeys, it is hypothesized that this behavior serves to repel insects and/or to mitigate topical skin infections (Baker 1996; Huffman 1997; DeJoseph et al. 2002). This is supported by the findings that, firstly, the frequency of occurrence of self-anointing correlated positively with humidity, which increases both the abundance of insects such as lice, ticks, and mosquitoes and the risk of bacterial or fungal skin infections (Baker 1996); secondly, the plant species used by capuchins for self-anointing contain secondary compounds known to have topical medicinal uses (DeJoseph et al. 2002), and thirdly, no difference between males and females in the frequency of selfanointing was observed (Baker 1996; Gilbert et al. 1998). Both capuchin monkeys and owl monkeys have also been reported to self-anoint with millipedes (Valderrama et al. 2000; Evans et al. 2003; Zito et al. 2003). These arthropods contain benzoquinones which have been demonstrated to repel insects (Weldon et al. 2003; Carroll et al. 2005). The only report of self-anointing in the genus Ateles so far (Campbell 2000) found free-ranging spider monkeys on Barro Colorado Island, Panama, to use three species of Rutaceae (Citrus aurantifolia, Zanthoxylum procerum, and Z. belizense) all of which are known to contain insect-repelling secondary compounds (Morton 1981; Downum et al. 1993). However, the findings that males displayed selfanointing significantly more often than females and a lack of seasonal variation in the frequency of occurrence of this behavior led the author to conclude that self-anointing in spider monkeys may serve a function
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other than to repel insects. This idea is also supported by the observation that the Panamanian spider monkeys rubbed the mixture of saliva and plant material only on the sternal and axillary regions of the body, which would be only of limited use to repel insects, whereas capuchins impregnate their entire body (Baker 1996). Among the three species of plants found in the present study that were used by free-ranging Mexican spider monkeys for self-anointing, only A. graveolens has been reported to contain insect-repellent compounds. In addition, extracts of this plant are used in traditional medicine as an anti-inflammatory agent and to combat fungal infections (Bown 1995). Similarly, leaf extracts of C. obtusifolia have been demonstrated in animal studies to exert analgesic, anti-inflammatory, and antibacterial activities and are widely used for these purposes in Latin America (Perez-Guerrero et al. 2001; Taylor 2005). The leaves of B. alamosana show antimyotoxic and anti-proteolytic properties and are therefore used against snakebites (Yetman and van Devender 2002), but to the best of our knowledge no other medicinal uses have been reported for this plant species. Although the possibility that the Mexican spider monkeys studied here used these plants to repel insects or to treat topical skin infections cannot be ruled out completely, this appears quite unlikely as, in agreement with the report on Panamanian spider monkeys (Campbell 2000), we observed self-anointing only in two group members, a lack of seasonal variation in the frequency of occurrence of this behavior, and application of the scent-bearing material only to a part of the body. Campbell (2000) proposed that self-anointing in Panamanian spider monkeys may serve a function in olfactory communication. Our observations that only adult males, one of them the highest-ranking individual of the group and father of the only infant, performed self-anointing, and that the leaves of all three plant species spread an intensive and aromatic odor when crushed, lend support to the idea that this behavior may be used in the context of social communication. Additionally, spider monkeys have been demonstrated to have a highly developed olfactory sensitivity both for plant-derived odorants (Hernandez Salazar et al. 2003; Laska et al. 2006a) and odorous steroids presumed to act as pheromones (Laska et al. 2005, 2006b). Future studies should therefore aim at testing this hypothesis experimentally and try to elucidate whether self-anointing in spider monkeys may perhaps play a role in signaling of social status or to increase sexual attractiveness.
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Primates (2007) 48:160–163 Acknowledgments We would like to thank Ernesto Rodriguez Luna, director in charge of the Parque de Flora y Fauna Silvestre Tropical, and Domingo Canales Espinosa, director of the Instituto de Neuro-Etologia of the Universidad Veracruzana, for their support.
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