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Owl Monkeys (Aotus spp.) Perform Self- and Social Anointing in Captivity
Abstract and Figures
Several species of primates, including owl monkeys (Aotus spp.), anoint by rubbing their fur with odiferous substances. Previous research has shown that capuchin monkeys (Cebus and Sapajus) anoint socially by rubbing their bodies together in groups of two or more while anointing. Owl monkeys housed at the DuMond Conservancy have been observed to anoint over the last 10 years, and we report detailed new information on the anointing behavior of this population, including descriptions of social anointing which occurs frequently. We first investigated the occurrence of self-anointing in 35 Aotus spp. presented with millipedes. Detailed descriptions regarding body regions anointed were obtained for all anointers (n = 28). The median duration for a self-anointing bout was 3.6 min (range from approx. 2 s to 14.15 min). While the latency and length of anointing bouts showed considerable interindividual differences, no statistically significant differences were found between sexes, wild- or captive-born owl monkeys or across age groups. However, we found the lower back and tail were anointed at a rate significantly greater than other body parts, but there were no differences in these patterns across sex or wild- or captive-born owl monkeys. More recently, social anointing was investigated in 26 Aotus spp. presented with millipedes, of which half were observed to anoint socially. The average duration for all social anointing bouts was 72.88 s, with a median duration of 30 s (range 5-322 s). A detailed ethogram was also generated that included behaviors that were performed while anointing, including facial expressions and vocalizations. The intraindividual variability for 8 monkeys used in both investigations is discussed. These findings extend our knowledge of anointing and confirm the existence of social anointing in another genus with a unique biology (nocturnal and socially monogamous) distinct from capuchins. © 2014 S. Karger AG, Basel.
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... The act of rubbing a material, object or foreign substance over different parts of the body is typically referred to as self-anointing (Baker 1996;Jefferson et al. 2014). This behaviour has been described in different taxa, including birds, carnivores and primates, and can be elicited by a wide variety of materials, such as plants, arthropods or humanmade products (Campbell 2000;Parkes et al. 2003;Weldon et al. 2006;Laska et al. 2007;Morrogh-Bernard 2008;Lynch Alfaro et al. 2012). ...
... In contrast, anointing with Rutaceae leaves by blackhanded spider monkeys (Ateles geoffroyi) and with Bauhinia leaves and flowers by titi monkeys (Callicebus sp.) has been suggested to have a social communicative function associated with scent marking (Campbell 2000;Souza-Alves et al. 2018). In these species, anointing is primarily observed among adult males, whereas anointing is shown by both sexes and different age classes in other species (Jefferson et al. 2014;Bowler et al. 2015;Gasco et al. 2016). In addition, in black-handed spider and titi monkeys, anointment was observed to be restricted to specific body areas commonly used for scent marking (sternal-axillary and chest-abdominal areas, respectively), whereas other species rubbed the entire body (Zito et al. 2002;Simmen and Tarnaud 2011;Jefferson et al. 2014;Bowler et al. 2015). ...
... In these species, anointing is primarily observed among adult males, whereas anointing is shown by both sexes and different age classes in other species (Jefferson et al. 2014;Bowler et al. 2015;Gasco et al. 2016). In addition, in black-handed spider and titi monkeys, anointment was observed to be restricted to specific body areas commonly used for scent marking (sternal-axillary and chest-abdominal areas, respectively), whereas other species rubbed the entire body (Zito et al. 2002;Simmen and Tarnaud 2011;Jefferson et al. 2014;Bowler et al. 2015). A social communicative function has also been suggested for lemurs because they appear to preferentially anoint the perianal area (Simmen and Tarnaud 2011). ...
Self-anointing, referring to the behaviour of rubbing a material object or foreign substance over different parts of the body,
has been observed in several vertebrate species, including primates. Several functions, such as detoxifying a rich food
source, social communication and protection against ectoparasites, have been proposed to explain this behaviour. Here, we
report observations of six wild red-fronted lemurs (Eulemur rufifrons) of both sexes and different age classes anointing their
perianal-genital areas and tails with chewed millipedes. Several individuals also ingested millipedes after prolonged chewing.
In light of the features of the observed interactions with millipedes, and the nature and potential metabolic pathways of the
released chemicals, we suggest a potential self-medicative function. Specifically, we propose that anointing combined with the
ingestion of millipedes’ benzoquinone secretions by red-fronted lemurs may act in a complementary fashion against gastrointestinal
parasite infections, and more specifically Oxyuridae nematodes, providing both prophylactic and therapeutic effects.
... Fur rubbing is not unique to capuchins, and may play an important role in the behavior of a number of Neotropical primates, including social interactions (Gilbert et al. 1998;Campbell 2000;Laska et al. 2007;Paukner and Suomi 2012;Jefferson et al. 2014;Huashuayo-Llamocca and Heymann 2017). Fur-rubbing behavior has been observed in Leontopithecus (Guidorizzi and Raboy 2009), Aotus (Zito et al. 2003;Jefferson et al. 2014), Plecturocebus (formerly Callicebus; Huashuayo-Llamocca and Heymann 2017), Callicebus (Souza-Alves et al. 2018), Saimiri (Nolte 1958;Fragaszy et al. 2004), Eulemur (Birkinshaw 1999;Peckre et al. 2018), andPongo (Morrogh-Bernard 2008). ...
... Fur rubbing is not unique to capuchins, and may play an important role in the behavior of a number of Neotropical primates, including social interactions (Gilbert et al. 1998;Campbell 2000;Laska et al. 2007;Paukner and Suomi 2012;Jefferson et al. 2014;Huashuayo-Llamocca and Heymann 2017). Fur-rubbing behavior has been observed in Leontopithecus (Guidorizzi and Raboy 2009), Aotus (Zito et al. 2003;Jefferson et al. 2014), Plecturocebus (formerly Callicebus; Huashuayo-Llamocca and Heymann 2017), Callicebus (Souza-Alves et al. 2018), Saimiri (Nolte 1958;Fragaszy et al. 2004), Eulemur (Birkinshaw 1999;Peckre et al. 2018), andPongo (Morrogh-Bernard 2008). The capuchins (Cebus and Sapajus), in particular, may benefit from the use of a wide range of materials, the exploitation of novel items, and the potential medicinal effects that some substances may have following the self-anointing (Westergaard and Fragaszy 1987;Valderrama et al. 2000;Weldon et al. 2003;Verderane et al. 2007;Bowler et al. 2015). ...
Fur rubbing or anointing is a well known behavior in capuchin monkeys (Cebus and Sapajus), and may have medicinal and/or social functions. Observations of anointing in capuchins have recorded the application of substances derived from both plants (orange, onion, garlic, citronella, and lemongrass) and animals (ants and millipedes). The present study reports on anointing behavior in free-ranging white-headed capuchins, Cebus capucinus, which involved a commercial insect repellent. After looting a bottle of repellent from the bag of a visitor to the Manuel Antonio National Park in Costa Rica, an adult male bit open the bottle and rubbed the leaking liquid over its entire body, focusing mainly on its belly. Other members of the group rubbed themselves against the male’s body and were eventually able to retrieve the bottle of repellent and anoint themselves. The repellent is composed mainly of extracts of eucalyptus and citronella. The capuchins may have been attracted by the strong citric scent of the citronella, which is known to stimulate fur-rubbing behavior in these monkeys. This is reinforced by the fact that the sequence of events was quite distinct from that associated with an earlier event, in which a juvenile male looted, tasted, and then discarded a stick of lip gloss and a tube of sunblock. Overall, the observations indicate that the citric scent of the repellent was attractive to the capuchins, especially in comparison with other man-made substances. As the animals partially ingested all the substances, there is clearly a need for more effective regulation of the contact between animals and visitors in the park.
... Alternatively, self-anointing may be a form of group scentmarking behaviour, just as urine washing, faecal marking and even the use of plant extracts in some primate species (Ueno, 1991;Campbell, 2000;Leca et al., 2007;Suomi, 2008, 2012). For instance, non-human primates such as spider (Ateles spp.), owl (Aotus spp.) and capuchin monkeys (Cebus and Sapajus) have been found to use selfanointing as a method of scent marking (olfactory communication or enhanced sociality) between individuals (Laska et al., 2007;Lynch-Alfaro et al., 2012;Jefferson et al., 2014). Given that individuals often interact with each other while self-anointing, this behaviour may reinforce social bonds and may be a form of social convention such as handclasp grooming in chimpanzees (McGrew and Tutin, 1978;Campbell, 2000;Carnegie et al., 2006;Laska et al., 2007;Leca et al., 2007;Suomi, 2008, 2012) and hand sniffing in white-faced capuchins (Perry et al., 2003). ...
... Neotropical primates have been recorded using olfactory cues to signal territorial, social and reproductive behaviours Heymann, 2006;Jefferson et al., 2014). According to Lynch-Alfaro et al. (2012), restricted locations on the body and lack of sociality for self-anointing behaviour could indicate that medicinal use is less likely to occur. ...
Self-anointing behaviour using Bauhinia sp. was reported in two captive titi monkeys (Callicebus coimbrai and
Callicebus barbarabrownae). The study was carried out from October 2013 to May 2014 during an experimental study
investigating the gut passage time of these individuals at the Getúlio Vargas Zoobotanical Park, North-eastern Brazil.
Although leaves, petioles and flowers of Bauhinia contain chemical substances that could affect the presence of
ectoparasites, it is unclear if titi monkeys demonstrate self-anointing behaviour as a method of self-medication. However,
due to the presence of large glands in C. coimbrai and C. barbarabrownae chests, and the high frequency of occurrence
observed for the adult male, we cautiously suggest that the use of Bauhinia may be linked to olfactory communication.
... Among mammals, orangutans (Pongo pygmaeus) rub leaf extracts with known anti-inflammatory properties onto specific parts of their body (Morrogh-Bernard 2008; Morrogh-Bernard et al. 2017), and capuchin (Sapajus and Cebus spp.) and owl monkeys (Aotus spp.) also anoint themselves and other social group members with a range of plant materials or crushed millipedes that possess antimicrobial, insecticidal, or other insect-repellent properties (Zito et al. 2003;Alfaro et al. 2012). Moreover, because capuchin and owl monkeys apply plant and invertebrate materials containing insect repellent and antimicrobial agents to areas that are particularly hard to groom, anointing behavior in these primate species is strongly indicative of a medicinal function (Jefferson et al. 2014;Bowler et al. 2015). While these studies lend support to the hypothesis that anointing with plant materials can be medicinal, it remains difficult to explain why female giant pandas were not observed to anoint with peppermint oil in the current study, because any medicinal function should apply equally to both sexes. ...
Although several mammals impregnate their fur with environmental odors, a phenomenon termed scent anointing or rubbing, the functional relevance of this behavior often is unclear. One theory is that scent anointing could be a form of scent matching with environmental odors to signal competitiveness and home range occupation. In this study we presented giant pandas with a range of odors to determine whether scent matching could provide a functional explanation for scent anointing in this species. We found that only a musk-based perfume elicited significantly more scent-anointing and scent-marking behavior than control. Males were also significantly more likely to scent-anoint and scent-mark than females. A preference for anointing, but not scent marking, when presented with peppermint (an insecticide) also was revealed. Our results suggest that giant pandas differentially scent-anoint with foreign odors to signal home range occupation, and possibly to repel ectoparasites. We also highlight how chemical signaling of resource-holding potential is likely to play an important role in determining competitive interactions between adult male giant pandas.
... For example, quilombolas have reported that when wounded by gunfire, howler monkeys and southern muriqui often use leaves, which they rub over or stuff into the wound. This is an ethnoecological record of what is known in the zoological literature as anointing or fur-rubbing behavior [97]. ...
Background:
As a leading practice of Homo sapiens' environmental experience for hundreds of millennia, hunting continues to evoke key research inquiries in the fields of archaeology, human ecology, and conservation biology. Broadly speaking, hunting has been mainly a subject of qualitative-symbolic and quantitative-materialistic schemata of analyze, among anthropologists and biologists, respectively. However, the phenomenological dimension of the hunting experience, in the course of individuals` everyday life, received little academic attention until this century. This study analyzes the daily praxis of hunting among quilombolas (descendants from runaway African slaves) in Southeast Brazil, making use of an ethnographic approach of phenomenological orientation, which dialogue with central ethnobiological issues. The authors also report the local ecological knowledge about mammals hunted in the area, and its relationship to the scientific literature on this subject.
Methods:
Between 2016 and 2019, the authors made use of participant observation and informal interviews among eight key local participants, in three quilombola communities in the Ribeira Valley (São Paulo, Brazil). Fragments of authors' field notes and parts of interviewers' speeches make up the core results obtained.
Results:
Articulating local knowledge to scientific literature, this study yielded a hybrid and comprehensive narrative about natural history of the mammals in the area. The authors also accessed elementary aspects of research participants' experience in hunting, such as strategies, tactics, motivations, and feelings. They reveal a set of human behavior dispositions that seems to emerge only in the context of the action, modulating the praxis of hunting on the course of individuals' everyday life.
Conclusion:
Ethnography, ethnobiology, and natural sciences backgrounds were systematically articulated in this research. This made possible to get a contextualized and multifaceted understanding of hunting praxis in the Ribeira Valley, an important socioenvironmental context of Atlantic Forest in Brazil. The role of an ethnographic approach applied to ethnoecological and biological conservation issues is especially considered here.
... Within primates, social anointing appears to be restricted to a few new world monkey taxa: the untufted capuchins (Alfaro et al., 2012) (Cebus), tufted capuchins (Alfaro et al., 2012) (Sapajus), and owl monkeys (Jefferson et al., 2014) (Aotus). Monkeys have been observed socially anointing using a variety of strongly smelling plants, mud, or insects which can be crushed into the fur or stimulated into secreting compounds (millipedes, stink bugs, ants) (Alfaro et al., 2012). ...
One of the striking features of human social complexity is that we provide care to sick and contagious individuals, rather than avoiding them. Care-giving is a powerful strategy of disease control in human populations today; however, we are not the only species which provides care for the sick. Widespread reports occurring in distantly related species like cetaceans and insects suggest that the building blocks of care for the sick are older than the human lineage itself. This raises the question of what evolutionary processes drive the evolution of such care in animals, including humans. I synthesize data from the literature to evaluate the diversity of care-giving behaviors and conclude that across the animal kingdom there appear to be two distinct types of care-behaviors, both with separate evolutionary histories: (1) social care behaviors benefitting a sick individual by promoting healing and recovery and (2) community health behaviors that control pathogens in the environment and reduce transmission within the population. By synthesizing literature from psychology, anthropology, and biology, I develop a novel hypothesis (Hominin Pathogen Control Hypothesis) to explain how these two distinct sets of behaviors evolved independently then merged in the human lineage. The hypothesis suggests that social care evolved in association with offspring care systems whereas community health behaviors evolved as a type of niche construction. These two types of behaviors merged in humans to produce complex, multi-level healthcare networks in humans. Moreover, each type of care increases selection for the other, generating feedback loops that selected for increasing healthcare behaviors over time. Interestingly, domestication processes may have contributed to both social care and community health aspects of this process.
... For example, quilombolas have reported that when wounded by gunfire, howler monkeys and southern muriqui often use leaves, which they rub over or stuff into the wound. This is an ethnoecological record of what is known in the zoological literature as anointing or fur-rubbing behavior [97]. ...
Background: As a leading practice of Homo sapiens´ environmental experience for hundreds of millennia, hunting continues to evoke key research inquiries in the fields of archaeology, human ecology and conservation biology. Broadly speaking, hunting has been mainly a subject of qualitative-symbolic and quantitative-materialistic schemata of analyze, among anthropologists and biologists respectively. However, the phenomenological dimension of the hunting experience, in the course of individuals` everyday life, received little academic attention until this century. This study analyzes the daily praxis of hunting among quilombolas (descendants from runaway African slaves) in Southeast Brazil, making use of an ethnographic approach of phenomenological orientation, which dialogue with central ethnobiological issues. The authors also report the local ecological knowledge about cinegetic mammals, and its relationship to the scientific literature on this subject. Methods: Between 2016 and 2019 the authors made use of participant observation and informal interviews among eight key local participants; in three quilombola communities in the Ribeira Valley (São Paulo, Brazil). Fragments of authors’ field notes and parts of interviewers’ speeches make up the core results obtained. Results: Articulating local knowledge to scientific literature, this study yielded a hybrid and comprehensive narrative about natural history of the cinegetic mammals in the area. The authors also accessed elementary aspects of research participants’ experience in hunting, such as strategies, tactics, motivations and feelings. They reveal a set of human behavior dispositions that seems to emerge only in the context of the action, modulating the praxis of hunting on the course of individuals’ everyday life. Conclusion: Ethnography, ethnobiology and natural sciences backgrounds were systematically articulated in this research. This made possible to get a contextualized and multifaceted understanding of hunting praxis in the Ribeira Valley, an important socioenvironmental context of Atlantic Forest in Brazil. The role of an ethnographic approach applied to ethnoecological and biological conservation issues is especially considered here.
Defensive secretions of millipedes are remarkable for containing toxic
quinones known to efficiently repell hematophagous arthropods. Here we show that
Endangered blonde capuchin monkeys make use of such secretions. We (i) describe the
anointing behavior performed by the monkeys (ii) identify the millipede species used
in the process (iii) describe the volatile chemical composition of its secretion.
The blonde capuchin monkeys selectively searched for millipedes hidden under the
ground. We observed three bouts of anointing behavior, performed by 13 individuals
of all age classes (from adults to independent infants), both solitarily (1 event)
and socially (10 events). The only millipede species used by the monkeys is an
undescribed species of the genus Poecilocricus
(Spirobolida, Rhinocricidae). The volatile chemical composition of the secretions
was predominantly comprised of a mixture of benzoquinones and hydroquinones. The
social nature of the behavior and time of the observations (mosquito season),
suggest that social bonding and mosquito avoidance is linked to the anointing
behavior of the monkeys.
Fur rubbing is a form of self-anointment in which pungent and/or physically stimulating substances are applied over the entire body in a stereotypical manner. Most widely reported among capuchin monkeys, it is also seen in other nonhuman primates. This behavior is thought to enhance fitness by reducing the risk of infection.
Self-medication in animals, (zoopharmacognosy) is the process by which wild animals use specific plants to combat disease or parasitic infections (Huffman, 2003; Jain et al., 2008). Zoopharmacognosy has been most widely studied in the African great apes with well-known examples including Pan troglodytes, Gorilla gorilla and Pan paniscus ingesting and defecating whole leaves to purge intestinal parasites (Huffman et al., 1996; Huffman, 1997; Huffman & Caton, 2001) and consuming potentially toxic plants with anti-parasitic properties (Clayton & Wolfe, 1993; Masi et al., 2012). In neotropical primates, examples of self-medication include Ateles belzebuth and Alouatta seniculus consuming soil at mineral licks (Link et al., 2011) and fur-rubbing with noxious invertebrates and strong smelling plants in Cebus and Sapajus species (Weldon et al., 2003; Leca et al., 2007; Lynch Alfaro et al., 2011), Ateles geoffroyi (Laska et al. 2007) and Aotus spp. (Jefferson et al. 2014). The majority of reports of self-medication in capuchins focus on fur-rubbing behaviours (Fragaszy et al., 2004; Paukner & Suomi, 2012; Meuner et al., 2008). Here, we report on observations of Hooded Capuchins in Rancho Laguna Blanca (RLB), feeding on the bark of the tree Albizia niopoides (Mimosaceae), a possible case of self-medication.
Songbirds apply ants to their feathers during anting behavior, possibly as a method of reducing feather parasites. We tested polar and nonpolar ant secretions and pure formic acid for bactericidal and fungicidal effects on microbial ectoparasites of feathers. Microbial inhibition trials were run with the bacteria Bacillus licheniformis (strains OWU 138B and OWU 1432B) and B. subtilis; and with the fungi Chaetomium globosum, Penicillium chrysogenum, and Trichoderma viride. Ant chemicals were derived from Camponotus pennsylvanicus, Pheidole dentata, Aphaenogaster rudis, Crematogaster lineolata, and Lasius flavus worker-caste ants. Although pure formic acid strongly inhibited all bacteria and fungal hyphae tested, concentrations of formic acid found in the bodies of formicine ants did not. Neither hexane ant-chemical extracts nor ant suspensions in deionized water inhibited the microbial species. Consequently, the hypothesis that birds apply ants to control feather parasites was not supported.
Twenty-eight specimens of the introduced diplopod Anadenobolus monilicornis (Spirobolida: Rhinocricidae) were collected in Key Largo, Florida and examined for parasitic intestinal nematodes. Two rhigonematid species, Heth mauriesi Adamson, 1982 and Ruizia karukerae Hunt, 1999 were discovered at 100% prevalence. The morphology of both species was verified by light and scanning electron microscopy. These species represent the first United States records for members of the genera Heth and Ruizia. The rich rhigonematid fauna in the Caribbean region, which has been documented on islands such as Cuba, Guadeloupe, and Puerto Rico, indicates the potential for future additional introductions of rhigonematids to North America.
Songbirds apply ants to their feathers during anting behavior, possibly as a method of reducing feather parasites. We tested polar and nonpolar ant secretions and pure formic acid for bactericidal and fungicidal effects on microbial ectoparasites of feathers. Microbial inhibition trials were run with the bacteria Bacillus licheniformis (strains OWU 138B and OWU 1432B) and B. subtilis; and with the fungi Chaetomium globosum, Penicillium chrysogenum, and Trichoderma viride. Ant chemicals were derived from Camponotus pennsylvanicus, Pheidole dentata, Aphaenogaster rudis, Crematogaster lineolata, and Lasius flavus worker-caste ants. Although pure formic acid strongly inhibited all bacteria and fungal hyphae tested, concentrations of formic acid found in the bodies of formicine ants did not. Neither hexane ant-chemical extracts nor ant suspensions in deionized water inhibited the microbial species. Consequently, the hypothesis that birds apply ants to control feather parasites was not supported.
Las aves paserinas aplican hormigas a sus plumas en el comportamiento de hormigueo, posiblemente como un método para reducir la carga parasitaria de las plumas. En este estudio probamos la capacidad bactericida y fungicida de secreciones polares y no polares de hormigas y formas puras de ácido fórmico sobre ectoparásitos microbianos de plumas. Las pruebas de inhibición bacteriana fueron realizadas con Bacillus licheniformis (cepas OWU 138B y OWU 1432B) y B. subtilis, y con los hongos Chaetomium globosum, Penicillium chrysogenum y Trichoderma viride. Los químicos de hormigas fueron derivados de las castas obreras de las especies Camponotus pennsylvanicus, Pheidole dentata, Aphaenogaster rudis, Crematogaster lineolata y Lasius flavus. A pesar de que las formas puras de ácido fórmico inhibieron fuertemente a todas las bacterias e hifas micóticas probadas, las concentraciones de ácido fórmico encontradas en los cuerpos de las hormigas de la subfamilia Formicinae no lo hicieron. Los extractos químicos de hexanos de hormigas y hormigas suspendidas en agua deionizadas tampoco inhibieron a las especies de microbios. Consecuentemente, la hipótesis de que las aves se aplican hormigas para controlar los parásitos de las plumas no fue apoyada.