American Journal of Primatology 69:706–712 (2007) BRIEF REPORT Ground Use by Northern Muriquis (Brachyteles hypoxanthus) ÍTALO M.C. MOURTHÉ1, DANUSA GUEDES2, JANAÍNA FIDELIS3, JEAN P. BOUBLI4, SÉRGIO L. MENDES5, AND KAREN B. STRIER6 1 Departamento de Zoologia, Instituto de Cieˆncias Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Brasil 2 Mestrado de Zoologia de Vertebrados, Pontifı´cia Universidade Católica de Minas Gerais, Belo Horizonte, Brasil 3 Pontifı´cia Universidade Católica de Betim-Minas Gerais, Belo Horizonte, Brasil 4 Department of Anthropology, University of Auckland, Auckland, New Zealand 5 Departamento de Cieˆncias Biológicas, Universidade Federal do Espı´rito Santo, Vitoria, Brasil 6 Department of Anthropology, University of Wisconsin-Madison, Madison, Wisconsin, USA Many arboreal primates descend to the ground, a custom that may occur more frequently in disturbed habitats, and in the presence of researchers to whom the primates are habituated. In this paper, we describe opportunistic observations of ground use in two groups of northern muriquis (Brachyteles hypoxanthus) at the RPPN Feliciano Miguel Abdala, Minas Gerais, Brazil. Members of both groups were observed drinking, resting, feeding, playing, and traveling on the ground to different degrees, and variation in the levels of habituation of the two groups may be responsible for the differences in the distribution of their terrestrial activities. The potential increase in vulnerability to predation or disease owing to ground use has implications for the conservation of this critically endangered species. Am. J. Primatol. 69:706–712, 2007. c 2007 Wiley-Liss, Inc. Key words: Northern muriquis; Brachyteles hypoxanthus; ground use; terrestriality; habituation; conservation INTRODUCTION The northern muriqui (Brachyteles hypoxanthus) is the largest member of the Atelidae family [but see Peres, 1994; Rosenberger & Strier, 1989]. It is arboreal and travels by means of suspensory locomotion. Like their close spider monkey relatives (Ateles spp.), the muriquis’ morphological adaptations for arboreality should make terrestrial locomotion inefficient [Campbell et al., 2005]. Similar to spider monkeys [Campbell et al., 2005] and howler monkeys [AlmeidaSilva et al., 2005; Bicca-Marques & Calegaro-Marques, 1995], muriquis are known Contract grant sponsor: The Zoological Society of San Diego/Conservation and Research for Endangered Species; Contract grant sponsor: The National Geographic Society, the Margot Marsh Biodiversity Foudation; Contract grant sponsor: The Liz Claiborne and Art Ortenberg Foundation; Contract grant sponsor: The Graduate School of the University of Wisconsin-Madison. Correspondence to: Karen B. Strier, Department of Anthropology, 1180 Observatory Drive, University of Wisconsin-Madison, Madison, WI 53706. E-mail: firstname.lastname@example.org. Received 10 July 2006; revision accepted 10 October 2006 DOI 10.1002/ajp.20405 Published online 25 January 2007 in Wiley InterScience (www.interscience.wiley.com). r 2007 Wiley-Liss, Inc. Muriqui Ground Use / 707 to traverse open areas on the ground, especially when habitat disturbances have isolated forest fragments or created gaps in the forest canopy [Dib et al., 1997; Lemos de Sá, 1988; Valle et al., 1984]. Increased terrestrial activities, especially in open areas, could increase the risks of predation [Takemoto, 2004; Terborgh, 1983], as well as of disease because of exposure to unfamiliar pathogens [Chapman et al., 2005]. In this paper, we compare patterns of ground use by two groups of northern muriquis in the same forest fragment. The groups currently utilize nonoverlapping home ranges, and differ in size and degree of habituation. We assume they are exposed to similar predation pressures, and therefore expected any differences in their ground use to correspond to ecological, demographic, or historical factors. METHODS The study was conducted at the RPPN Feliciano Miguel Abdala (previously known as the Estac- ão Biológica de Caratinga), located in Minas Gerais, Brasil (191 500 S; 411 500 W). The 957 ha forest fragment is characterized by sub-montane semideciduous Atlantic forest vegetation [Oliveira-Filho & Fontes, 2000]. The climate is seasonal, with 480% of the 1119.87262.75 mm of annual rain falling between October and March [Dias & Strier, 2003]. The forest has a history of substantial disturbance, and only a small fraction could be considered undisturbed [Hatton et al., 1984]. Historical agricultural clearings, selective logging, fire, and hunting have altered the mammalian community, and many larger species, such as peccaries (Tayassu pecari), tapir (Tapirus terrestris), jaguar (Pantera onca), and puma (Puma concolor) that once occurred in this area are locally extinct [Ferrari, 1988; Hatton et al., 1984]. Nonetheless a community of potential predators still exist in this reserve, including tayra (Eira Barbara), ocelot (Leopardus tigrinus), and some larger falconiformes (Leptodon cayanensis and Spizastur melanoleucus) [Bianchi, 2001; Ferrari, 1988; Printes et al., 1996; Strier, 1999]. Although the smaller of these species may not pose predation risks to adult muriquis, it is likely that solitary infants or juveniles could be easy prey for them [Printes et al., 1996]. In addition, we have heard and observed feral dogs in the forest while accompanying our study groups, and the muriquis routinely give alarm calls when the dogs are nearby. Opportunistic data were collected whenever ground use was observed in two muriqui groups (Jáo and Matão Groups) during the course of systematic studies focused on other aspects of their behavior. Observations of the Jaó Group, which occupies the northern part of the reserve, were made between May 2002 and September 2003 and in May 2004, when it included up to 100 individuals and frequently subdivided into smaller parties. Observations on the Matão Group, whose home range encompasses the southern part of the reserve, were made from November 2004 through May 2005 when the group included 80 individuals. Both study groups are fully habituated to the presence of observers, but they differ considerably in the length of time they have been monitored. The Matão Group was observed sporadically by researchers since the 1970s, and has been followed intensively since 1983. The location of the Matão Group’s home range also puts its members in greater contact with local people than the Jaó Group, which occupies a more remote part of the forest [Valle et al., 1984]. Although researchers have also observed the Jaó muriquis since the 1970s, the first systematic study on this group was initiated in 2001 [Strier & Boubli, 2006]. Am. J. Primatol. DOI 10.1002/ajp 708 / Mourthé et al. Both of the groups were accompanied on a near daily basis during their respective study periods, resulting in 245 observation days over the 18-month period with the Jaó Group, and 159 observation days during the 7-month period with the Matão Group. For the purposes of our analyses, we define an observation day as one on which a minimum of 8 h of visual contact with at least one member of a group was maintained. We defined a terrestrial event as one in which one or more individuals of either group was observed to descend to the ground, or sighted when already on the ground, until all individuals returned to the trees. For each event, all activities (e.g., drinking water, resting, feeding, traveling, or socializing) were recorded. We analyzed ground use by events, regardless of the number of individuals recorded in any observation. If more than one activity occurred during a terrestrial event, the activities were scored as equal proportions. Accidental ground uses such as falls from trees were excluded. We calculated monthly rates of ground use on the basis of the total number of observation days for each group during each month. Non-parametric statistical tests were used because the data were not normally distributed. We considered Po0.05 to indicate a statistically significant difference between groups. RESULTS A total of 88 ground use events were observed on 54 different days. The Jaó Group accounted for 35 ground use events on 27 of the 245 observation days; the Matão Group accounted for 53 ground use events on 27 of the 159 observation days. Monthly rates of ground use were significantly higher for the Matão Group (Mean7SD 5 0.1770.12 events, N 5 7 months, median 5 0.12, range 5 0.06–0.38) than for the Jaó Group (0.0870.14 events, N 5 18 months, median 5 0.03, range 5 0–0.53 events; Mann–Whitney U 5 27, Po0.05). Both groups were observed to drink water, rest, feed, travel, and socialize while on the ground (Fig. 1). Drinking accounted for a significantly greater Fig. 1. Distribution of observed terrestrial activities by both groups. Jaó Group in black (N 5 35 events) and Matão Group in white (N 5 53 events). The asterisks indicate statistically significant differences, as described in the text. There were no significant differences in the percentage of ground use events devoted to feeding (w2 5 0.11, df 5 1, P40.05), traveling (w2 5 3.24, df 5 1, P40.05), or socializing (w2 5 0.24, df 5 1, P40.05). Am. J. Primatol. DOI 10.1002/ajp Muriqui Ground Use / 709 percentage of ground use events in the Jaó Group than in the Matão Group (w2 5 20.5, df 5 1, Po0.001), whereas resting accounted for a significantly greater percentage of the Matão Group’s ground use (w2 5 8.04, df 5 1, Po0.001). DISCUSSION In contrast to previous anecdotal accounts of ground use by muriquis at our study site [Dib et al., 1997, 2001; Strier, 1999; Valle et al., 1984], we found that muriquis now engage in a variety of activities, only some of which, such as drinking water, could be attributed to necessity. Moreover, we found significant differences in both the rate of ground use events and the distribution of terrestrial activities by the two groups. These findings suggest that ground use is currently more common than previously observed, reflecting the effects of habituation to researchers, as well as the effects of loss of large predators, such as jaguars, at the study site. Individuals in both groups descended to the ground to drink water from streams. The majority of ground use events observed in the Jaó Group involved drinking during the dry season, when water was less likely to be available in tree boles [Strier, 1999]. We do not know whether there were any seasonal differences in ground use in the Matão muriquis because most observations of that group were made during the rainy season. However, rates of ground use by the Jaó muriquis were lower during the rainy than the dry season, similar to the seasonal patterns of terrestrial activities reported in chimpanzees (Pan troglodytes) [Takemoto, 2004; Wrangham, 1977]. Resting accounted for approximately 30% of the ground use events observed in the Matão Group during this study, a highly atypical behavior for an arboreal primate. Terrestrial resting was only observed on one occasion by a single individual in the Jaó Group, which perhaps not coincidentally was an adult female known to have emigrated from the Matão Group. Terrestrial feeding events involving soil consumption have previously been reported for the Matão Group [e.g., Dib et al., 2001], and were observed in both groups in the present study. In addition, we observed muriquis feeding on the bark of an unidentified liana, as well as on mature fruits of two species of shrubs, Palicourea tetrapylla and Psychotria warmingii (Rubiaceae). Muriquis were also observed to feed on the mature fruits of tree species, including Genipa americana that had fallen. The scarcity of fruits in the understory and on the ground may restrict terrestrial feeding events for the more frugivorous spider monkeys [Campbell et al., 2005], but for muriquis, large concentrations of fallen fruits appear to be an attraction. This may be especially or exclusively true in disturbed forests, such as our study site, where large frugivorous mammals (e.g., tapirs, white-lipped peccaries) are extinct. All of the terrestrial travel events observed during our study involved short distances (2–15 m), and most occurred in areas of local habitat disturbance. Terrestrial travel is the only way for arboreal primates to move between forest fragments [Bicca-Marques & Calegaro-Marques, 1995; Johns, 1986]. An adolescent female muriqui in another population was captured when she was attempting to traverse a pasture separating the 44 ha forest inhabited by her natal group [Lemos de Sá, 1988]. In our study, however, all of the instances of terrestrial travel by muriquis could have been easily avoided because of the short distances covered and the availability of alternative arboreal routes. Similar cases of unnecessary terrestrial travel have also been observed in sympatric brown Am. J. Primatol. DOI 10.1002/ajp 710 / Mourthé et al. howler monkeys (Alouatta guariba clamitans) in the Matão Group’s home range [Almeida-Silva et al., 2005]. On one occasion, a subgroup of adult male muriquis in Jaó descended to travel a few meters on the ground, seemingly to avoid a confrontation with another subgroup of males that was resting in the trees above. On another occasion, an adolescent female that had recently immigrated into the Jaó Group descended to the ground in what appeared to be an attempt to escape from a resident adult female who was chasing her. Other cases of terrestrial travel during social interactions, such as that during an intergroup confrontation, were also observed in the Matão Group more than 20 years ago [Strier, 1999]. Muriquis in both study groups engaged in affiliative social interactions on the ground. In the Jaó Group, adults socialized on the ground less often than immatures, which were observed to play in localized areas, chasing one another while moving back and forth between the ground and vegetation during the interactions. Adults in the Matão Group socialized more frequently on the ground than adults in the Jaó Group. The more frequent and varied ground use by the Matão Group compared to the Jaó Group may be due to its longer habituation to human observers. A similar increase in ground use with increasing habituation has been observed in other primates at Santa Rosa National Park, Costa Rica [Campbell et al., 2005]. Interpopulation differences in predation risks may also account for variation in the ground use behavior of arboreal primates. For example, Campbell et al.  suggest that the lower frequency of ground use by Ateles belzebuth compared to A. geoffroyi could be attributed to the size and composition of the predator populations in their respective communities. Similar to Ateles spp., the muriquis in our study population appeared to be vigilant when on the ground. Any loud noise or unusual disturbance led to their immediate return to the trees and elicited alarm calls. Although tayra (Eira larbara) are primarily arboreal predators, one was suspected of taking an infant muriqui from the Matão Group on the ground [Printes et al., 1996], and muriqui fur has been found in the scats of ocelot (Leopardus pardalis) at this site [Bianchi, 2001]. It is difficult, nonetheless, to evaluate the effects of predators on muriqui ground use patterns because in other larger, less disturbed forests with larger predator populations, such as at Parque Estadual do Rio Doce, Brazil, muriquis have also been observed to descend to the ground to consume soil and drink water [Luiz G. Dias, personal communication]. However, non-essential behaviors such as resting or playing on the ground have not yet been observed here, consistent with the idea that a decrease in perceived predation risk may be behind the optional ground use by arboreal monkeys. Muriquis at our field site may also be vulnerable to attacks by feral dogs. Galetti and Sazima  reported black-horned capuchins (Cebus nigritus) and brown howler monkeys (Alouatta guariba) being killed by feral dogs in another forest fragment of southern Brazil while they were traveling on the ground between forest gaps. Feral dogs have also been reported to harass primates, including northern muriquis, in the small forest fragment at Fazenda Esmeralda, some 100 km from our study site [Melo et al., 2005]. The potential increased risks of terrestrial predation may be offset by the deterring effects that the presence of researchers may have on the predators [Isbell & Young, 1993]. However, arboreal primates that become accustomed to descending to the ground when observers are present may persist in this behavior when researchers, and their predator-deterrent effects, are absent. Am. J. Primatol. DOI 10.1002/ajp Muriqui Ground Use / 711 Ground use may also expose habitually arboreal primates to unfamiliar parasites or other pathogens that could contribute to disease. A wide array of diseases and infections can be transmitted by direct or indirect contact with humans [Woodford et al., 2002]. At our field site, there may also be risks from contact with the dung of domestic livestock and feral dogs that defecate in areas that the primates also use when they descend to the ground. The trade-offs between habituating arboreal primates for observational research that can benefit conservation efforts may inadvertently increase their vulnerability to both predators and disease if habituation leads to increased terrestriality. We suggest that researchers be attentive to these risks, particularly when initiating new field studies on endangered arboreal species. ACKNOWLEDGMENTS We thank the Brazilian government and CNPq for permission to conduct this research, Abdala family for permission to work at their reserve, and CI-Brasil for infrastructure. We also thank Fabiano Andrade and Wanderson Silva for their field assistance with the Jaó Group. We are grateful to Paul Garber and two anonymous reviewers for their helpful suggestions and comments. 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