Fur rubbing, i.e. rubbing a substance or an object into
the pelage, has been described in numerous Neotropical primate species,
including species of titi monkeys, but it seems to be a rare behaviour. Here we describe a fur rubbing event in a wild coppery titi monkey
(Plecturocebuscupreus) with Psychotria sp. (Rubiaceae) leaves observed and videotaped during a field study on vigilance behaviour between September–December 2019 in the Peruvian
Amazon. Plants of the genus Psychotria contain a great diversity of secondary metabolites and are often used in traditional medicine. We suggest that the fur rubbing was an act of self-medication. This is the first record of fur rubbing in coppery titi monkeys in almost 4400 h of observation accumulated over more than 20 years.
Introduction
Nonhuman primates are known to manipulate non-food items they find in their
surroundings and to ingest or apply them to their bodies. Such items
include various plant parts, minerals, arthropods or man-made products (e.g.
soap) (Baker, 1996; Bowler et al., 2015; Huffman, 1997; Pebsworth et al., 2021; Peckre et al., 2018). The ingestion or topical use of these items can serve as social communication or for self-medicative purposes, also known as
zoopharmacognosy (Rounak et al., 2011). For example, in white-faced capuchin
monkeys (Cebuscapucinus) collective fur rubbing has been proposed as a way to socialise
with other group members (Baker, 1996; Leca et al., 2007). In most cases,
however, fur rubbing is performed individually and considered
self-medication in a broad sense, i.e. a behaviour used for ectoparasite
removal, repelling insects, treating skin infections and wounds, soothing or
stimulating the skin or even as fur conditioning (Baker, 1996; Gibson, 1990;
Mascaro et al., 2022; Westergaard and Fragaszy, 1987). Plant parts can be
rubbed into the fur directly or after squeezing or chewing them (Huffman,
1997). Such plant part manipulation probably leads to the release of
secondary compounds, which can then be applied onto the fur more easily when
mixed with saliva (Huffman, 1997). Fur rubbing has been observed in a number
of primate species, both in the wild and in captivity (e.g. Baker, 1996;
Campbell, 2000; Laska et al., 2007; Morrogh-Bernard et al., 2017; Zito et al., 2003). Observations of fur rubbing in different species of titi monkeys are
summarised in Table 1.
A summary of fur rubbing with leaves observed in titi monkeys. NA:
information not available.
Titi monkey speciesPlant species (family)Mode of leafDurationApplication onSourcehandling(s)body areaPlecturocebus discolorTetrathylacium sp. (Salicaceae)chewingNANACarrillo-Bilbao et al. (2005)Plecturocebus toppini (formerly Callicebusbrunneus)Undetermined species from Annonaceae and BignoniaceaechewingNAabdominal areaFrancis Bossuyt, per- sonal communication in Carillo-Bilbao et al. (2005)Callicebus coimbrai and CallicebusbarbarabrownaeBauhinia sp. (Fabaceae)squeezing with one or both hands15–30chest and abdominal areaSouza-Alves et al. (2018)Plecturocebus oenanthe (formerly Callicebusoenanthe)Piper aduncum (Piperaceae)squeezing with both hands300–900chest and abdominal areaHuashuayo-Llamocca and Heymann (2017)Plecturocebus brunneusSenna obtusifolia (Fabaceae), Piper tuberculatum (Piperaceae)chewingNAchestOliveira et al. (2020)Plecturocebus cupreusPsychotria sp. (Rubiaceae)chewing∼ 300abdominal areathis report
Here we describe, for the first time, an event of fur rubbing by a coppery
titi monkey (Plecturocebuscupreus) in the Peruvian Amazon.
Methods
The observation was made during a study at the Estación Biológica
Quebrada Blanco (EBQB), a study site in the northeastern Peruvian Amazon
(4∘21′ S, 73∘09′ W), some 90 km south southeast of
Iquitos. For details of the study area see Heymann et al. (2019).
We observed four groups of coppery titi monkeys as part of a study on
vigilance between September–December 2019. Group 4, in which we observed the
fur rubbing behaviour, consisted of one adult male, one adult female and
their subadult offspring. Observations were usually made from dawn (06:00 PET, Peru time), when the group left their sleeping site, until almost dusk (17:00 PET), when they retreated to one. Throughout the study, we used instantaneous scan sampling of 2 min for standardised data collection and ad libitum sampling for
recording unusual events (Altman, 1974).
Results
On the 12 November 2019 at 12:04 PET, the adult male of the group
climbed down a liana and, stopping at the height of less than 2 m, ripped a
handful of leaves from a Psychotria sp. (Rubiaceae) understory tree. Then he climbed
back up the liana, sat down and started chewing on the leaves. Then he took
the leaves out of his mouth and rubbed them slowly but firmly on his lower
abdomen (Video supplement). He continued this action for about 5 min. Then he discarded the leaves and moved towards the group, which had remained < 5 m away during the event.
Discussion
We report here the first case of fur rubbing behaviour by a coppery titi
monkey using the leaves of Psychotria sp. in the Peruvian Amazon. Based on the
similarity in the mode of application of the chewed leaves on the body
reported in other primates, we suggest a self-medicative function to the
behaviour of the coppery titi monkey. In the absence of a species level
plant identification, we cannot suggest a specific medicinal mechanism in
titi monkeys.
Our interpretation of a self-medicative function is supported by the fact
that species of Psychotria (one of the largest angiosperm genera with about 1650
species; Nepokroeff et al., 1999), which have been chemically analysed,
include a diversity and considerable concentrations of secondary compounds.
These compounds show cytotoxic, analgesic, antiviral and antifungal
bioactivities (Calixto et al., 2016). This makes Psychotria popular in traditional
medicine and as herbal medicinal products, used topically in cases of skin
disorders, ocular disorders, to relieve fever, headaches and earaches (Calixto et al., 2016). The species identity could not be determined unambiguously, and
therefore it is impossible to tell whether this specific plant is used in
folk medicine. However, a number of Psychotria species are used in Amazonian (and Central and South American) ethnobotany (Benevides et al., 2005; Duke and Vasquez, 1994; see Table S1 in the Supplement). Therefore, it can be reasonably assumed that the plant used by the titi monkey could have some medical properties, too. Although Psychotria can include psychoactive tryptamines that show
hallucinogenic activity (McKenna et al., 1984), this is unlikely to account
for fur-rubbing, as oral uptake is required for this effect. Our on-field
examination of the plant revealed the crushed leaves to have a cinnamon-like
scent of ground leaves.
The observation has been made in November during the onset of the rainy
season. Although the number of ectoparasites, like mosquitoes and ticks,
might have been on the increase, Psychotria spp. are not known to have insect repellent properties. Restricting application to the abdominal part of the body is also not compatible with this explanation (Koyama et al., 2008; Simmen and Tarnaud, 2011).
Interestingly, this behaviour has been observed for the first time at the
EBQB, despite almost 4400 h of observing coppery titi monkeys between
1997–2019. Obviously, it is a rare behaviour, which makes any interpretation
difficult. Further detailed behavioural observations and identification of
the plant species used are needed before the function of the behaviour can
be conclusively determined. Only through the accumulation of this kind of
anecdotal observations will it be possible to detect more general patterns
that can lead to more conclusive interpretations.
Ethical statement
This work was conducted with all necessary permits (research permit no. 249-2017-SERFOR/DGGSPFFS from the Servicio Nacional Forestal y de Fauna Silvestre of the Peruvian Ministry of Agriculture) and adhered to the IPS Code of Best Practices for Field Primatology.
Data availability
Data sharing is not applicable to this article as no datasets were generated or analysed during the current study.
Video supplement
A video that documents the observed fur rubbing is available on 10.5446/56632 (Theara et al., 2022).
The supplement related to this article is available online at: https://doi.org/10.5194/pb-9-7-2022-supplement.
Author contributions
GKT collected the data; JRM and RZG identified the plant; GKT, EWH and SD wrote the paper.
Competing interests
The contact author has declared that neither they nor their co-authors have any competing interests.
Disclaimer
Publisher’s note: Copernicus Publications remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Acknowledgements
We are thankful for Camilo Flores Amasifuén and Migdonio Huanuiri
Arirama for their assistance during our field surveys. We are also grateful
to Michael A. Huffman and an anonymous reviewer, who provided us with valuable comments on earlier versions of the manuscript.
The study on titi monkeys at EBQB was authorised by the Servicio Forestal y
de Fauna Silvestre (SERFOR) of the Peruvian Ministry of Agriculture (permit
no. 249-2017-SERFOR/DGGSPFFS).
Review statement
This paper was edited by Dietmar Zinner and reviewed by Michael Huffman.
References
Altmann, J.: Observational study of behavior: sampling
methods, Behaviour, 49, 227–266, 1974.Baker, M.: Fur rubbing: use of medicinal plants by capuchin monkeys (Cebus capucinus), Am. J. Primatol., 38, 263–270, 1996.Benevides, P. J. C., Young, M. C. M., and Bolzani, V. D. S.: Biological activities of constituents from Psychotria spectabilis, Pharm. Biol., 42, 565–569, 10.1080/13880200490901780, 2005.Bowler, M., Messer, E. J., Claidière, N., and Whiten, A.: Mutual
medication in capuchin monkeys–Social anointing improves coverage of
topically applied anti-parasite medicines, Sci. Rep., 5, 1–10,
10.1038/srep15030, 2015.Calixto, N. O., Pinto, M. E. F., Ramalho, S. D, Burger, M., Bobey, A. F., Young, M. C. M., Bolzani, V. S., and Pinto, A. C.: The genus Psychotria: Phytochemistry, chemotaxonomy, ethnopharmacology and biological properties, J. Brazil. Chem. Soc., 27, 1355–1378, 10.5935/0103-5053.20160149, 2016.Campbell, C. J.: Fur rubbing behavior in free-ranging black-handed spider
monkeys (Ateles geoffroyi) in Panama, Am. J. Primatol., 51, 205–208, 2000.Carrillo-Bilbao, G., Di Fiore, A., and Fernández-Duque, E.: Dieta,
forrajeo y presupuesto de tiempo en cotoncillos (Callicebus discolor) del Parque Nacional Yasuní en la Amazonia Ecuatoriana, Neotropical Primates, 13, 7–11, 2005.
Duke, J. A. and Vasquez, R.: Amazonian ethnobotanical dictionary, Boca
Raton, CRC Press, ISBN 0-8493-3664-3, 1994.Gibson, K. R.: Tool use, imitation, and deception in a captive cebus monkey, in: “Language” and intelligence in monkeys and apes: Comparative developmental perspectives, edited by: Parker, S. T. and Gibson, K. R.,
Cambridge University Press, 205–218, 10.1017/CBO9780511665486.009,
1990.Heymann, E. W., Culot, L., Knogge, C., Smith, A. C., Herrera, E. R. T.,
Müller, B., Stojan-Dolar, M., Ferrer, Y. L., Kubisch, P., Kupsch, D.,
Slana, D., Koopmann, M. L., Ziegenhagen, B., Bialozyt, R., Mengel, C.,
Hambuckers, J., and Heer, K.: Small Neotropical primates promote the natural
regeneration of anthropogenically disturbed areas, Sci. Rep., 9,
1–9, 10.1038/s41598-019-46683-x, 2019.Huashuayo-Llamocca, R. and Heymann, E. W.: Fur-rubbing with Piper leaves in the San Martín titi monkey, Callicebus oenanthe, Primate Biol., 4, 127–130, 10.5194/pb-4-127-2017, 2017.
Huffman, M. A.: Current evidence for self-medication in primates: A
multidisciplinary perspective, Am. J. Phys. Anthropol., 104, 171–200, 1997.Koyama, N., Aimi, M., Kawamoto, Y., Hirai, H., Go, Y., Ichino, S., and Takahata, Y.: Body mass of wild ring-tailed lemurs in Berenty Reserve, Madagascar, with reference to tick infestation: a preliminary analysis, Primates, 49, 9–15, 10.1007/s10329-007-0051-4, 2008.Laska, M., Bauer, V., and Salazar, L. T. H.: Self-anointing behavior in
free-ranging spider monkeys (Ateles geoffroyi) in Mexico, Primates, 48, 160–163, 10.1007/s10329-006-0019-9, 2007.Leca, J. B., Gunst, N., and Petit, O.: Social aspects of fur-rubbing in
Cebus capucinus and C. apella, Int. J. Primatol., 28, 801–817, 10.1007/s10764-007-9162-4, 2007.
Mascaro, A., Southern, L. M., Deschner, T., and Pika, S.: Application of
insects to wounds of self and others by chimpanzees in the wild, Curr.
Biol., 32, R112–R113, 2022.McKenna, D. J., Towers, G. H. N., and Abbott, F.: Monoamine oxidase inhibitors in South American hallucinogenic plants: tryptamine and β-carboline constituents of ayahuasca, J. Ethnopharmacol., 10, 195–223, 1984.Morrogh-Bernard, H. C., Foitová, I., Yeen, Z., Wilkin, P., De Martin, R.,
Rárová, L., Doležal, K., Nurcahyo, W., and Olšanský, M.:
Self-medication by orang-utans (Pongo pygmaeus) using bioactive properties of Dracaenacantleyi, Sci. Rep., 7, 1–7, 10.1038/s41598-017-16621-w, 2017.Nepokroeff, M., Bremer, B., and Sytsma, K. J.: Reorganization of the genus
Psychotria and tribe Psychotrieae (Rubiaceae) inferred from ITS and rbcL sequence data, Syst. Bot., 24, 5–27, 10.2307/2419383, 1999.Oliveira, B. L. P., Souza-Alves, J. P., and Oliveira, M. A.: Potential self-medication by brown titi monkeys, Plecturocebus brunneus, in an urban fragment forest in the Brazilian Amazon, Primate Biol., 7, 35–39, 10.5194/pb-7-35-2020, 2020.
Pebsworth, P. A., Gruber, T., Miller, J. D., Zuberbühler, K., and Young,
S. L.: Selecting between iron-rich and clay-rich soils: a geophagy field
experiment with black-and-white colobus monkeys in the Budongo Forest
Reserve, Uganda, Primates, 62, 133–142, 10.1007/s10329-020-00845-y, 2021.Peckre, L. R., Defolie, C., Kappeler, P. M., and Fichtel, C.: Potential
self-medication using millipede secretions in red-fronted lemurs: combining
anointment and ingestion for a joint action against gastrointestinal
parasites?, Primates, 59, 483–494, 10.1007/s10329-018-0674-7, 2018.
Rounak, S., Apoorva, K., and Shweta, A.: Zoopharmacognosy (animal self
medication): a review, International Journal of Research in Ayurveda and
Pharmacy, 2, 1510–1512, 2011.Simmen, B. and Tarnaud, L.: Utilisation des sécrétions de
myriapodes chez les lémurs et les sapajous: fonction curative ou
signalisation sociale?, Revue de primatologie, 3,
10.4000/primatologie.644, 2011.Souza-Alves, J. P., Albuquerque, N. M., Vinhas, L., Cardoso, T. S., Beltrão-Mendes, R., and Jerusalinsky, L.: Self-anointing behaviour in captive titi monkeys (Callicebus spp.), Primate Biol., 5, 1–5, 10.5194/pb-5-1-2018, 2018.Theara, G. K., Ruíz Macedo, J., Zárate Gómez, R., Heymann, E. W., and Dolotovskaya, S.: Fur rubbing in Plecturocebus cupreus – an incidence of self-medication?, TIB AV-Portal [video], 10.5446/56632, 2022.Westergaard, G. and Fragaszy, D.: Self-treatment of wounds by a capuchin
monkey (Cebus apella), Human Evolution, 2, 557–562, 1987.Zito, M., Evans, S., and Weldon, P. J.: Owl monkeys (Aotus spp.) self-anoint with plants and millipedes, Folia Primatol., 74, 159–161,
10.1159/000070649, 2003.