Use of Medicinal Plants by Capuchin Monkeys (Cebus Capucinus)

American Journal of Primatology 38263-270 (1996)

Fur Rubbing: Use of Medicinal Plants by Capuchin Monkeys (Cebus capucinus)

MARY BAKER Department of Anthropology, University of California, Riverside There is a growing body of evidence documenting animals’ selective use of medicinal plants found in their environments. During research conducted in Costa Rica, capuchin monkeys (Cebus capucinus) have been observed topically applying material of at least four plant genera (Citrus,Clematis, Piper, and Sloanea). The first three of these plants contain secondary compounds which are known to have anti-insect andfor medicinal benefits and the ethnographic record shows that indigenous peoples throughout the New World use these plants for similar purposes and in similar ways. It is suggested that free-ranging nonhuman primates use plants topically for their potential medicinal purposes. o 1996 WiIey-Liss, Inc. Key words: Cebus, fur rubbing, self-anointment, medicinal plant use, ethnobotany

INTRODUCTION There is an increasing interest in, and documentation of, medicinal plant use by nonhuman primates. Several articles have described the ingestion of plant material to relieve intestinal and other maladies [see Rodriguez & Wrangham, 1993; Wrangham & Goodall, 19891. This paper will describe the topical application of plant material and other substances by capuchin monkeys [see also Buckley, 1983; Gibson, 1990; Hill, 1960; Longino, 1984; Nolte, 1958; Oppenheimer, 1968; Ritchie & Fragaszy, 1988; Westergaard & Fragaszy, 19871.

METHODS During August and September 1991 and January through June 1993 research was conducted on white-faced capuchin monkeys (Cebus capucinus) at the Curd Refugio de Vida Silvestre in Costa Rica, located on the south-eastern edge of the Nicoya Peninsula. A total of 1,140 field hours were logged, 660 dry season hours (January-April) and 480 wet season hours (MaySeptember). During 2 week periods in January, February, and March 1993, I worked with a colleague and three Earthwatch teams. All data from the 1991 field season and the remainder of the 1993 field season were collected by me. Observations were conducted from 06:OO until 18:OO on four troops ranging in

Received for publication May 3, 1994; revision accepted September 15, 1995. Address reprint requests to Mary Baker, Department of Anthropology, University of California, River- side, CA 92521.

0 1996 Wiley-Liss, Inc. 264 I Baker

- -~ .

I- Citrus Clematis Piper Sloanea Unknown

Fig. 1. Plant species used by the capuchin monkeys at Curu and the number of bouts they were observed being used. Since more than one plant genus could be used within a single bout, the total number of times all plant genera were used (n = 62) does not equal the total number of bouts (n = 53). size from 11 to 32 members. Hourly records were kept of ambient conditions and troop location. In addition to methods used to record social and foraging behaviors, ad libitum accounts of all occurrences of “fur rubbing” behavior were recorded. Fur rubbing was defined as the rubbing of foreign substances into the fur (see below). When possible, recorded information included a description of how the plant was used, which part of the plant was used, duration of the behavior, the number and identification of participants, and if they were alone (solitary) or in contact with one another (social). Plant specimens were collected for later identification at the University of California, Riverside, herbarium. A fur rubbing bout was defined as the period of time starting when an individual in the troop began using plant material and ending when the last individual in the troop concluded the behavior. Intervals greater than 10 min when no rubbing was observed constituted a new bout. A bout could involve a single individual or the entire group. Data was collected on individuals participating within a bout and the data are analyzed according to what individuals did; e.g., within a single bout there could be durational scores for five individuals. RESULTS The capuchins were observed fur rubbing with at least four, and possibly five, different plant genera during the research period (Fig. 1).They used the fruit of several introduced species of Citrus. They also used the seed pods of one tree, “terciopelo” (Sloaneu terniflora, Elaeocarpaceae), and the leaves andlor stems of three vines: “barba de viejo” (Clematis dioica L.), “anise” (Piper marginatum Jacq.), and one unidentified species. The application of plant material was highly energetic, almost frenzied in appearance. The monkeys moved rapidly, drooling, biting into the plant and rolling it between their hands. Then, using their hands, feet, and tails, they applied the plant material over various body parts or over their entire bodies. When using citrus fruit, sometimes only the rind was used. They first abraded it by biting or rolling and pounding the fruit on tree branches and then applied it over the body Fur Rubbing by Capuchin Monkeys / 265

Fig. 2. Adult male applying C~trusjuice over his body. He has pounded the fruit on the tree and is digging into it. He will then apply the juice over his body using his hands, feet, and tail.

(Fig. 2). More commonly, however, after pounding the fruit on tree branches, the monkeys broke open the fruit to extract the pulp and juice. The monkeys hugged the fruit to their chests and stomachs while simultaneously rubbing it, digging into it, and rubbing it into their fur, usually covering the entire body. The monkeys selected the fuzzy pods of the “terciopelo” (Sloanea ternifloru) tree to rub over their bodies. When most of the hairs which cover the pods had been rubbed off, they selected new fuzzy pods to rub with. The stems of Clematis and leaves of Piper and an unidentified vine species were manually or orally broken up into small pieces and rubbed between the monkeys’ hands. They mixed their saliva with the plants, presumably to facilitate application, and rubbed the mixture into their fur in the same energetic manner. Fifty-three fur rubbing bouts were recorded (Fig. 1). Although bouts of fur rubbing usually involved one plant type (45 bouts), in some cases there were two (seven bouts) or three (one bout) plant genera used during a single bout. Citrus was used more frequently than the other plant genera: the capuchins were observed rubbing Citrus into their fur during 33 bouts, and it was used exclusively during the dry season. The use of vines was not as common; Clematis was used in 11 bouts and Piper in 15. Sloanea was used once. I was unable to locate the plant used in two bouts. Twelve fur rubbing bouts were observed during the dry season (f = O.OlS), and 41 were seen during the rainy season (f = 0.085) (Fig. 3). There is a significant difference in the number of bouts that occurred during dry and wet seasons (x2 = 15.8, P 5 0.05). Time spent fur rubbing by individuals ranged from less than 10 sec to as much as 41 min; the mean durational score for all individuals was 6.3 min. Fur rubbing usually corresponded with foraging behavior; if a plant was encoun- 266 I Baker

50 i

40 T 0 t a 30- I

B 0 20- U t S 10 -

Dry Season Wet Season

Fig. 3. Total number of observed fur rubbing bouts during the dry and wet seasons.

tered, the monkeys might stop to use it. On three separate occasions, however, individuals or small groups left the main troop to find citrus to rub into their fur. Fur rubbing bouts could involve a single monkey (“individual rubbing”), small groups, or the entire troop. When groups fur rubbed, some individuals were not in contact with others (“solitary rubbing”) while others engaged in what was termed “social fur rubbing.” The monkeys huddled together in small groups ranging in size from two to seven. Those with plant material applied it in the usual manner. Those without plant material rubbed the plants held by those who had them, or picked up dropped pieces to rub over their bodies. Alternatively, those without plant material would rub their bodies over and in between those who had plant material. The result was a mass of wet, drooling monkeys with bits of citrus pulp and juice or broken leaves sticking to their fur, squirming and rolling over and around each other. Seven individual fur rubbing bouts were recorded. Of the 46 bouts which involved groups, 17 involved solitary rubbing only, six involved social rubbing only, and 23 included both solitary and social fur rubbing.

DISCUSSION There is a substantial body of ethnographic literature from around the world describing the medicinal uses of Citrus, Clematis, and Piper. Although all medicinal uses of these plants are important, I will restrict this survey to topical medicinal uses of these plants in Latin America. As can be seen in Table I, these plants are used by people for a number of skin problems. These plant genera are also known to contain a number of secondary compounds which have topical medicinal uses (Table 11). Chemical analysis of P. marginatum, collected from the Amazon and Trinidad, has found that there are many medicinally useful compounds in this species [see Maxwell & Rampersad, 1988; Ramos et al., 19861. It is possible that the monkeys are using these plants for similar reasons, or, at the very least, they may be benefitting from similar medicinal affects of these plants. There does not appear to be anything written on the chemical compounds of the seed pods of Sloanea or information regarding medicinal uses of this genus. It has been noted that the leaves are not attacked by insects, which suggests that the Fur Rubbing by Capuchin Monkeys / 267 TABLE I. Topical Ethnomedicinal Uses of the Fruit of Citrus sp. and the Leaves and Stems of Clematis dioica and Piper marginaturn in Mexico and Central and South America* Citrus limona (Lemon) Antibacterial, disinfectant, dermic counterirritant Mexico: poultice, antiseptic, pain killer, rub on insect bites Citrus aurantiifolia (Lime) Tropical Middle America: a disinfectant for the eyes of newborn infants, hemostat for nosebleeds Trinidad: treatment for erysipelas Bahamas: repels mosquitos, relieves itching mosquito bites Citrus sznensis (Sweet orange) Bactericide Citrus aurantium (Sour orange) Poultice for sores, fungistatic Caicos Islands: poulticed on sores Citrus reticulata (Mandarin orange) Fungistatic, bactericide Clematis dioica (“Barba de viejo”) Mexico: treatment for skin ailments of both humans and animals, removes skin blemishes and freckles Guatemala: a rubefacient and blistering agent, relieves fever Puerto Rico: a rubefacient, removes freckles and skin blemishes Cuba: for rheumatism Brazil: for rheumatism Piper marginatum (“Anise”) Puerto Rico: hemostat, especially for excessive menstrual flow Panama: treatment for catarrh, fever Surinam: wash wounds Trinidad for influenza

*Data from Bianchini and Corbetta L19751, Messegue 119791, Morton [19811, Nunez Melendez [19821, Schultes and Raffauf 119901, and van Reis Altschul [19731. leaves contai powerful secondary compounds [Janzen, 19831. The ti y purple hairs which cover the seed pods are known to be irritating to the human skin [Collins et al., 19901. It is curious that the monkeys selectively favor pods with hair, discarding them after the hairs have been wiped off to choose more with hair. It is possible that the hairs are not irritating to their skin; what humans find to be irritating may be pleasurable or stimulating to the monkeys. It is also possible that the monkeys’ fur prevents the Skoanea hairs from penetrating their skin and irritating it. It will be interesting to discover what chemicals are present on the hairs and if they have anti-insect or other medicinal uses. There are two qualities that are consistent among all items selected by the monkeys for fur rubbing (Table 111). First, they favor items that are pungent such as Citrus, Piper, tobacco, onion, garlic, alcohol, formic acid, ants, and millipedes [Buckley, 1983; Gibson, 1990; Hill, 1960; Longino, 1984; Nolte, 1958; Oppenhei- mer, 19681. Citrus is especially favored according to many accounts; one captive 268 I Baker

TABLE 11. Phytopharmaceutical Properties and Known Medicinal Effect in Citrus, Clematis, and Piper Genus Phytocheinical Effect“ Citrus sp.” Benzaldehyde Anesthetic Carvone Insecticide Cresol Antiseptic Furfural Fungicide, germicide. insecticide Linalool Antimicrobial Narcotine Antitussivr I’yrocatechol Antiseptic Quercitrin Viricide Terpineol Antiallergic. antiasthmatic, antitussive, bacteriostatic CZe tt 1 a ti sli Anemonin Bactericide Methyl salicylatc Andgesic , anti-i nf‘l arn ma t ory Piper” Anethole Insect icicle Apiole Insecticide Cineole lnsectifuge Dihydrokawain Anesthetic, anti-inflnmmntory Eugenol Analgesic. antiseptic, anesthetic, fungicide. larvicide Safrole Anrhthetic, antiseptic -______~

This list includes only the c(inip~ruiicIstin. t~liichdfvcts ww knnu 11 Ibr ttipiciil application+. Thcw is one other known compound in C‘/iwati,s. and there iil’ii many ni(11’~~cnmp~iuiids cnnt;tined in (’ilrits and Pipw ”Data from Duke 11986. Tnhles :3 and 41. monkey enjoys fur rubbing with lemon so much as to include all lemon-scented things including lemon-flavored Gummi Bears (Sarah Boysen, personal communication, 1992). The second criterion contains substances that are “stimulating” when rubbed into their fur, including Citrus juice, Clematis (a rubefacient), and ice. It may be that they like the feel of these things on their skin (Dorothy Fra- gaszy, personal communication, 1992). Fur rubbing seems similar to “anting” behavior seen in some birds and mam- mals IChisholm, 1959; Hauser, 1964; Potter, 19701, wherein live ants are placed on the body or allowed to crawl over it. Other types of insects, plant material, and other substances are also used. There are several explanations for this behavior, but the three most commonly discussed are that it may remove ectoparasites, it may be soothing or stimulating to the skin, or it may condition the fur or feathers. It is noteworthy that anting tends to increase during periods of high humidity [Chisholm, 1959; Potter, 1970 I. This behavior also seems similar to the use of pungent vegetation in nest building by some species of passerine birds. Since these birds may be at increased risk of infection due to prolonged or repeated nest use, these plants may rid the nest of bacteria, parasites, and microbes which could be harmful to the fledglings [see Clark & Mason, 1985, 19871. There are several hypotheses which might explain fur rubbing. The monkeys may know that these plants have medicinal uses and select them for this purpose. It would be expected that the behavior would increase during the wet season when the heat and high humidity might increase the risk of bacterial and fungal infections. Two accounts in the literature suggest a medicinal benefit from this behavior. Gibson I1990 I described a captive capuchin monkey who was prone to necrotic skin infections that regularly required treatment,. He was provided tobacco on a daily basis which eliminated future skin infections. Westergaard and Fragaszy (19871 report the application of maple syrup directly onto wounds by an adult Fur Rubbing by Capuchin Monkeys I 269 TABLE 111. Qualities of Items Used by Capuchin Monkevs for Fur Rubbing* Plant Pungent Stimulating Citrus spp." Y' Y Clematis dioica N Y Sloanea terniflora N Y Piper spp. Y N Diffenbachia ~p.~ ? ? Annona ~p.~ ? ? Tobaccod Y N Onionsd Y N Garlicd Y N Iced N Y Millipedes" Y ? Ants' Y ? Alcoholg Y Y Formic acidg Y ? *See also Rodriguez and Wrangham [19933. "S. Boysen, personal communication 119921; Buckley [I9831 bOppenheimer [19681. 'Y = yes; N = no; ? = possible or unknown. dGibson [19901. "D. Fragaszy, personal communication L19921. fHill 119601, Longino [19841, Nolte [19581. gHill [19601. female, who was later observed treating her infant's wounds [Ritchie & Fragaszy, 19883. The intent of the monkeys, however, when applying these plants may not be for medicinal purposes. The scents of these plants may serve to establish a group scent, much the way that urine washing and other forms of scent marking do for other primates. Social fur rubbing may be similar to grooming, in that it may serve to reinforce social ties. They may simply enjoy the interaction with the plant material as cats enjoy catnip. CONCLUSIONS 1. Capuchin monkeys (Cebus sp.) are known to apply plant matter, insects, and other substances topically, all of which are pungent smelling and/or stimulating when applied to the skin. 2. Capuchins in Costa Rica use Citrus fruit and the stems of Clematis, leaves of Piper, and seed pods of Sloanea for fur rubbing. 3. The behavior is seen more often in the wet season than in the dry season. 4. These plants possess medicinally useful chemicals and are used by peoples in Latin America to relive skin problems. ACKNOWLEDGMENTS I thank Scott Fedick, Jim Moore, Alan Fix, and the four anonymous reviewers for their suggestions in the writing of the manuscript. I thank Dusty Becker and the volunteers of the 1993 Earthwatch program for their hard work and support. Dr. Arturo Gomez-Pompa, Dr. William Berger, and Andrew Sanders provided the botanical identifications. I am very grateful to the Schutt-Valle family, Dona Juli- eta, Adelina, Frederico, and Luis, for welcoming me into their home, for all their help, and especially for their enthusiasm and commitment to the understanding 270 I Baker and conservation of wildlife. 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