acta ethol (2010) 13:137139 DOI 10.

1007/s10211-010-0068-3

SHORT COMMUNICATION

Interspecific association between an ungulate and a carnivore or a primate

Arnaud Lonard Jean Desbiez & Fabiana Lopes Rocha & Alexine Keuroghlian

Received: 24 June 2009 / Revised: 24 September 2009 / Accepted: 16 March 2010 / Published online: 12 May 2010 # Springer-Verlag and ISPA 2010

Abstract In the Brazilian Pantanal, we observed collared peccaries (Pecari tajacu) associating with South American coatis (Nasua nasua) 13 times and three times with black howler monkeys (Alouatta caraya). The scansorial coati drop fruit whilst feeding that both collared peccaries and other coatis consume. Young coatis were also observed chewing on the pulp left over from seeds spat out by collared peccaries who had removed the hard exocarp. Both species react to each other s alarm calls. Peccaries also benefited from the fruits dropped by black howler monkeys. Ecologically, coatis are omnivores; but taxonomically, they are carnivores. To our knowledge, the collared peccary/coati association is the first report of an interspecific association between an ungulate and a carnivore. Keywords Alouatta caraya . Frugivore . Interspecific association . Mixed species groups . Nasua nasua . Pecari tajacu
Electronic supplementary material The online version of this article (doi:10.1007/s10211-010-0068-3) contains supplementary material, which is available to authorized users. A. L. J. Desbiez (*) Royal Zoological Society of Scotland, Murrayfield, Edinburgh EH12 6TS, Scotland, UK e-mail: adesbiez@hotmail.com F. L. Rocha Programa de Ps-graduao em Biologia Parasitria-Fundao Oswaldo Cruz, Avenida Brasil, 4365 Manguinhos Pavilho Rocha Lima, Rio de Janeiro, Brazil A. Keuroghlian Wildlife Conservation Society, Brazil, Rua Jardim Botnico, 674 Rio de Janeiro, Brazil

Mixed species groups can occur among different species of mammals ranging from closely related species to species from different orders. They can take place in different habitats ranging from ungulates in open grasslands (FitzGibbon 1990; Sinclair 1985), primates in forests (Chapman and Chapman 2000) to cetaceans in the oceans (Frantzis and Herzing 2002). Mixed species groups are usually restricted to social species that normally live together in groups (Stensland et al. 2003). These groups can be very different in their duration, frequency and predominant activity and structure, depending on which species are interacting (Cords 1987). In general, these associations offer both foraging advantages and predator avoidance benefits (Stensland et al. 2003). We report observations of associations between collared peccaries Pecari tajacu (Linnaeus 1758) and a carnivore, the South American coati Nasua nasua (Linnaeus 1766) as well as the association between collared peccary and a primate species, the black howler Alouatta caraya (Humboldt 1812), in the central region of the Brazilian Pantanal wetland. Between July 2002 and October 2004, a study on the density of medium- to large-sized mammals (>1 kg) was conducted in a central region of the Brazilian Pantanal (18 59 S, 56 39 W) using line transect methods in a 200-km2 area which included six traditionally managed cattle ranches (Desbiez et al. 2010). During this field work, we observed collared peccaries associating with South American coatis and howler monkeys. Collared peccary groups were sighted from the trails foraging, travelling or resting together with groups of South American coatis on 11 occasions (Table 1). During this study, groups of collared peccaries were sighted 120 times from the trail and groups of South American coatis 305 times. Two other opportunistic observations of collared peccary and coatis also occurred, and on both occasions, the animals were foraging together on Attalea phalerata (Arecaceae) (Mart.) fruits. Interspecific associations between

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collared peccaries and coatis occurred in different habitats, and in 80% of the sightings from the trail, the animals were foraging together (Table 1). Collared peccaries have also been observed consuming fruit dropped by howler monkeys. In the study area, a group of howler monkeys was being studied and followed daily (da Cunha 2005). At one point during the research, collared peccaries came several days in a row to consume Agonandra brasiliensis (Opiliaceae) (Miers) fruits under the same tree in which a group of howler monkeys was feeding. The collared peccaries arrived and left at the same time as the howler monkeys for five consecutive days (da Cunha, personal communication). On two other occasions, a group of collared peccaries was sighted foraging under a fig tree (Ficus sp., Moraceae) on the fruits dropped by howler monkeys. During the line transect study, no interspecific association between collared peccaries and howler monkeys was observed even though howler monkeys were sighted 116 times from the trail. However, fruit availability in the Pantanal is very seasonal so fruiting of species favoured by howler monkeys can easily be missed from the trails. For example, A. brasiliensis fruits are available for only a month while mature A. phalerata fruits, which are not consumed by howler monkeys, are available for 7 months (Desbiez 2007). There are therefore more opportunities to observe collared peccaries engaging in interspecific associations when foraging on A. phalerata fruits. It can be difficult to distinguish a mixed species group from an aggregation. Mixed species groups can also be the result of two species moving independently, but responding in a similar way, to a resource and when doing so they can form an interspecific group (Waser 1982, 1984). The definition of mixed species associations in the literature is often very broad or even lacking. The narrowest definition proposed by Stensland et al. (2003) defines mixed species associations where two or more species are seen in such
Table 1 Observations of interspecific associations between collared peccary (CP) and coatis (C) in the central region of the Brazilian Pantanal

close association that they can be regarded as members of the same group. This was never the case with the collared peccary associations, which were much looser gatherings. The definition of mixed species associations used here must be interpreted in its broadest sense. Because the primary objective of the study was estimating mammal densities, the duration of the associations was not systematically timed. The association between collared peccaries and coatis appeared to have both anti-predator and foraging advantages. Both collared peccaries and other coatis consume fruit at the foot of the tree that the scansorial coati drop while feeding. Collared peccaries gained a foraging advantage by associating with coati groups, but coatis also benefit when foraging A. phalerata seeds with peccaries. Young coatis are unable to open the hard exocarp of A. phalerata fruits to reach the nutritious pulp. However, they were observed chewing on the pulp left over from seeds spat out by collared peccaries. Young coatis conserve energy and obtain a more efficient utilisation of the food resource that they would be otherwise unable to access. Similarly, we observed collared peccaries chewing on fruits previously chewed on by the coatis. The video provided in the supplementary materials (link to video) shows collared peccaries foraging on A. phalerata fruits dropped by South American coatis from the crown of a A. phalerata palm tree. In this video the collared peccary eats a fruit previously rid of its exocarp by the coati above, it then eats a fruit dropped by a coati; finally, a young coati is seen chewing on a fruit previously masticated by a collared peccary that is also without its exocarp. The animals filmed were observed travelling and foraging together at several palm trees for more than an hour. When we left, the animals were still together. Another functional explanation for mixed species groups of coatis and collared peccaries may be predator detection. The total number of eyes and ears available to detect predators

Group size CP 2 7 3 3 10 1 7 5 2 4 5 C 20 8 11 12 9 4 11 12 6 6 9 Habitat Scrub grassland Forest Open grassland Open grassland Open grassland Alkaline pond Forest Scrub forest Forest Forest Forest Behaviour Foraging fruit from Byrsonima orbignyana Travelling and foraging through Bromelia balansae Foraging at the edge of pond Foraging at the edge of pond Foraging at the edge of dry pond Travel/forage around alkaline pond Foraging A. phalerata fruits Travel Resting Eating buds and flowers unidentified tree Foraging A. phalerata fruits

acta ethol (2010) 13:137139

139 Acknowledgements Funding for this work was provided by the European Union INCO PECARI project, Embrapa Pantanal and the Royal Zoological Society of Scotland (RZSS).

is increased in a mixed species group, and consequently, allowing each animal to spend less time being vigilant (Cords 1987). In addition, a mixed species group can be more efficient in the detection of predators if the two different species use different senses or abilities to scan for predators (Heymann and Buchanan-Smith 2000). Collared peccaries and coatis have different abilities to detect predators and we have observed both coatis and collared peccaries react to each others alarm calls. The observer walking the transects had higher chance of being detected by mixed species groups than by single species groups. When travelling in the open grasslands and foraging at the edge of ponds, an increased number of different animals may offer important antipredator advantages. The howler monkey/collared peccary association was always due to concentrated resources. During these encounters, the peccaries benefited from the fruits dropped by the monkeys. The monkeys did not benefit from the presence of the peccaries in any obvious way. In Venezuela, similar associations between collared peccary groups and troops of capuchin monkeys Cebus olivaceus (Schomburgk 1848) have been reported (Robinson and Eisenberg 1985). In that study monkeys were observed overhead collared peccaries on 39 of 86 encounters, and each encounter peccary were consuming fruits shaken and dropped by the monkeys (Robinson and Eisenberg 1985). Associations between collared peccary and howler monkeys in the Pantanal were much less frequent. In the literature, mixed species groups comprising different ungulate species are common. Gazelles Eudorcas thomsonii (Gunther 1984), zebras Equus quagga (Boddaert 1785) and wildebeest Connochaetes taurinus (Burchell 1823) are famous for associating in mixed species groups on the Serengeti plains (FitzGibbon 1990; Sinclair 1985). Ungulates have also been reported to associate with primates, and interspecific associations between monkeys and deer are commonly reported in Asia (Majolo and Ventura 2004; Newton 1989). Ecologically, coatis are omnivores; but taxonomically, they are carnivores. To our knowledge, the collared peccary/South American coati association is the first report of an interspecific association between an ungulate and a carnivore.

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