American Journal of Primatology 69:11731178 (2007)

RESEARCH ARTICLE Ocelot (Leopardus pardalis) Predation on Primates in Caratinga Biological Station, Southeast Brazil
RITA DE CASSIA BIANCHI AND SERGIO LUCENA MENDES Universidade Federal do Esprito Santo, Esprito Santo, Brazil

This study demonstrates that ocelots (Leopardus pardalis) extensively use primates as a food resource at the Caratinga Biological Station (CBS) in Southeast Brazil. Analysis of 60 fecal samples collected over 4 years revealed predation upon the brown howler monkey (Alouatta guariba), the muriqui (Brachyteles hypoxanthus), and the brown capuchin monkey (Cebus apella). The most frequent items found in the fecal samples analyzed were Calomys (n 5 16) and non-identied Aves (n 5 15), followed by A. guariba (n 5 12). Although Rodentia was the most common group consumed (n 5 52) Primates were found in 27% of total fecal samples and were the third most consumed group in relation to the total items. Particularly, predation of A. guariba by ocelots (20% of the total fecal samples) was not an isolated event; our results showed that this species was preyed on across several months. Predation on primates was far higher at CBS than at other sites where comparable studies have been carried out. Am. J. Primatol. 69:11731178, 2007.
c

2007 Wiley-Liss, Inc.

Key words: predation; Neotropical felids; ocelot; brown howler monkey; diet

INTRODUCTION The major primate predators are mammalian carnivore and raptors. Whereas every group of predator potentially takes both terrestrial and arboreal primates, there seems to be a tendency toward greater vulnerability of arboreal primates to raptors, whereas terrestrial primates are more vulnerable to mammalian carnivores [Boinski et al., 2000]. Neotropical primates may be more frequently predated by birds than by carnivore mammals. The modication of the primates behavior by the potential presence of aerial predators indicates that raptors represent an important predatory threat to primates [Heymann, 1990; Vasquez & Heymann, 2001]. In southwestern Guyana, remains found under the nest of the Harpia harpyja corresponded to 18 individuals of four species of primates
Correspondence to: Rita De Cassia Bianchi, Programa de Pos-Graduacao em Biologia Animal, - pe Vitoria, Esprito Universidade Federal do Esprito Santo. Av. Marechal Campos, 1468, Maru Santo, Brazil. E-mail: rc_bianchi@yahoo.com.br

Received 23 May 2006; revised 1 December 2006; revision accepted 21 December 2006 DOI 10.1002/ajp.20415 Published online 28 February 2007 in Wiley InterScience (www.interscience.wiley.com).

r 2007 Wiley-Liss, Inc.

1174 / Bianchi and Mendes

(Cebus sp., Alouatta seniculus, Pithecia pithecia and Chiropotes satanas) [Retting, 1978]. Vasquez and Heymann [2001] report on two successful attacks by crested eagles, Morphnus guianensis, on infant Saguinus mystax and S. fuscicollis and argue that since twin births are the rule in callitrichines but populations do not grow drastically, a large proportion of infants and juveniles is probably lost to predators. Miranda et al. [2006] recorded antipredatory behaviors (N 5 9) of brown howlers (A. guariba clamitans) under attack by the black hawk-eagle (Spizaetus tyrannus). In Africa, where the primate predation record are better documented, several remains of bones and skulls of the primates are identied in nest of raptors [Karpanty, 2006; McGraw et al., 2006; Sanders et al., 2003] and raptors are a major class of predators of anthropoid primates, being signicant predators of cercopithecoid monkeys throughout the sub-Saharan region [Skorupa, 1989]. In Neotropical forests, the top mammalian predators are felids, which prey mainly upon terrestrial mammals [Crawshaw, 1995; Emmons, 1987; Ludlow & Sunquist, 1987; Moreno et al., 2006]. Arboreal mammals such as primates are also prey of felids, but documentation and quantication of the extent of primate predation is scanty. The few studies reporting the predation of primates by felids included only inferences about probable predation by felids [Peetz et al., 1992] or few samples of scat or stomach contents [Beebe, 1925; Miranda et al., 2005; Ximenez, 1982]. The ocelot, Leopardus pardalis, is among the mammalian predators of primates. These medium-sized (815 kg) cats are opportunistic hunters that feed primarily on small mammals but also take larger preys, such as red brocket deer (Mazama americana), collared peccaries (Pecari tajacu) or howler monkeys (A. caraya) [Murray & Gardner, 1997]. Nonetheless, ocelot diet remains largely unknown throughout most of the Neotropics, while some studies cast some light on the extent of predation on primates [Emmons, 1987; Moreno et al., 2006], there is little understanding of the potential predation risk that ocelots represent to primates. In this paper, we report ocelot predation on primates, especially on the brown howler monkey (A. guariba), through scats in southeast Brazil. These data suggest that felids represent signicant threats to primates in the New World as well as the Old World. METHODS From January 1997 to September 2000, we opportunistically collected fecal samples of ocelot along roads and trails in the Caratinga Biological Station (CBS) (191500 S and 41150W), Minas Gerais, Brazil. The CBS (957 ha) is a Private Reserve of Natural Patrimony [Castro, 2001; Fonseca, 1989]. Vegetation ts the Low-Montane Atlantic Fluvial Forest, with characteristics of semi-deciduous to deciduous forests [Hirsch, 1995]. Climate, based on Koppens classication, is tropical sub-hot mild humid (AW), with an average temperature equal to 16.51C in the coldest month (July) and 23.91C in the hottest month (February). The dry season presents 132.8 mm of precipitation, whereas the wet season presents 839.2 mm. There is no information on the population of ocelots or any other mammal carnivores in the region, although many species have been seen by researches in the study area, such as Cerdocyon thous and Leopardus wiedii; likewise, several scat samples of domestic dogs have been collected.

Am. J. Primatol. DOI 10.1002/ajp

Ocelot (Leopardus pardalis) Predation on Primates / 1175

Ocelot diet was determined from the collection and analysis of scats. Scats were identied as derived from ocelots based on an association with tracks, as well as the presence of ocelot hairs that were likely ingested during self-grooming. The hairs were identied through cuticle and medulary patterns [Quadros, 2002]. The scats were oven dried and washed on a sieve. The screened material (e.g., hair, teeth, and scales) was identied by comparison with the material deposited at the Zoological Collection of Prof. Mello Leitao Biology Museum (Santa Teresa, Esprito Santo), through analysis of the guard-hair microstructure [Quadros, 2002], or by consultation with a specialist. Prey use was assessed as frequency of occurrence of items in the total of fecal samples (% fecal samples) and as percentage of occurrence of items in the total of items (% items). The presence of an item was considered to represent a single individual, except in the case of teeth, where the minimum number of individuals consumed was evaluated from the number of teeth found in the sample. Plants were not considered as an item as felids usually consume grass [Emmons, 1987; Moreno et al., 2006]. RESULTS A total of 60 fecal samples were collected and analyzed (n 5 56 in the dry season and n 5 4 in the wet season). The brown howler monkey (A. guariba 4.17.2 kg), the muriqui (Brachyteles hypoxanthus1215 kg), and the brown capuchin monkey (Cebus apella1.74.5 kg) accounted, respectively, for 9.7, 2.4, and 0.8% of the total items found. A. guariba was the third most consumed item (10% of the total items found), being present in 20% of the total fecal samples (Table 1). With relation to total scats the most important item was Calomys (n 5 16). Rodentia was the most important group consumed (n 5 52), with Calomys sp. being found in 16 of the fecal samples. Non-identied Aves (n 5 15) was the second most frequently found item, followed by Primata, which represented 27% of the fecal samples and was the third most consumed group in relation to the total items (Table 1). The brown howler monkey was predated in different months during years 1997, 1998, and 1999, showing that predation of this species was not an isolated, but a relatively frequent event. Moreover, by examining the number of the samples in each month, we observed that there were at least seven different predation events of brown howler monkeys, one of muriquis, and one of brown capuchin monkeys. DISCUSSION Emmons [1987] and Ludlow and Sunquist [1987] inferred that the ocelot is specialized in preying on small animals. However, the predation of small animals could be related to their relative abundance. Moreover, the diversity of the diet of the ocelot is demonstrated both by the consumption of items ranging from crabs to deer (Mazama spp.) and by its opportunistic behavior through the consumption of the most abundant items [Crawshaw, 1995; Ludlow & Sunquist, 1987]. In similar studies, only in Peru [Emmons, 1987], Southeast Brazil [Bianchi, 2001], and Panama [Moreno et al., 2006] primates were consumed by ocelots, but at low rates. Other reports are based on the analysis of stomach content in Bolivia [Ximenez, 1982] and in Guyana [Beebe, 1925], but no study has identied ocelot predation on primates to the extent observed at CBS.

Am. J. Primatol. DOI 10.1002/ajp

1176 / Bianchi and Mendes

TABLE 1. Prey Items Found in 60 Samples of Ocelots Scats at Caratinga Biological Station Item Rodentia Calomys sp. Sphiggurus sp. Rodentia n.i. Bolomys sp. Oligoryzomys sp. Cuniculus paca Akodon sp. Guerlinguetus aestuans Cavia sp. Trinomys sp. Sigmodontinae n.i. Didelphimorphia Monodelphis americana Didelphidae n.i. Didelphis aurita Gracilinanus sp. Primates Alouatta guariba Brachyteles hypoxanthus Cebus apella Cingulata Dasypus sp. Lagomorpha Sylvilagus brasiliensis Mammalia n.i Aves Aves n.i. Squamata Ophidia n.i. Lacertilia n.i. Ameiva ameiva Tupinambis merianae Teiidae n.i. Invertebrates Plants
a

N 52 16 10 6 5 4 3 3 2 1 1 1 20 6 6 4 4 16 12 3 1 7 7 3 3 2 15 15 9 4 2 1 1 1 11 20 124

% scats 86.68 26.67 16.67 10.00 8.33 6.67 5.00 5.00 3.33 1.67 1.67 1.67 33.34 10.00 10.00 6.67 6.67 26.67 20.00 5.00 1.67 11.67 11.67 5.00 5.00 3.33 25.00 25.00 15.01 6.67 3.33 1.67 1.67 1.67 18.33 33.33

% items 41.94 12.90 8.06 4.84 4.03 3.23 2.42 2.42 1.61 0.81 0.81 0.81 16.14 4.84 4.84 3.23 3.23 12.91 9.68 2.42 0.81 5.65 5.65 2.42 2.42 1.61 12.10 12.10 7.27 3.23 1.61 0.81 0.81 0.81 100%

N, number of occurrence of each item; % scats, occurrence frequency of the item in the total of scats; % items, percentage of occurrence of an item in the total of items. a Main vertebrata taxa consumed are in bold type.

The high consumption of the brown howler monkey in CBS may be related to the high densities of this prey species and its relative vulnerability. Population density estimates of brown howler monkey in CBS are 0.91.4 per hectare [Hisrch, 1995]. Brown howler monkeys in CBS are found in groups of about six individuals (typically one male, two or three females, and cubs) and they have young individuals all year round [Strier et al., 2001]. Their main defense strategy is to take refuge in secluded places in the foliage and to perform agonistic vocalization [Mendes, 1989]. While resting, they stay at a height of 1520 m, but they use the whole strata (020 m) for feeding purposes, and frequently come to the ground for drinking water (personal observations). It is relatively uncommon

Am. J. Primatol. DOI 10.1002/ajp

Ocelot (Leopardus pardalis) Predation on Primates / 1177

for New World primates to come to the ground, although it has been noted that some platyrrhines such as Ateles eat soil or rotten wood, visit salt licks and drink water from streams during the dry season [Campbell et al., 2005]. How would ocelots prey upon primates? Primates in general could escape predation simply by climbing to the highest part of the tree. Ocelot hunting strategy might be similar to that of the leopard (Panthera pardus); the cats climb trees, causing primates to panic to the point that some will leap to lower branches and then to the ground where they are easily taken [Dunbar, 1923 and Pocock, 1939 in Sunquist & Sunquist, 2002]. The predation of the brown howler monkey can be an isolated event, performed by a single individual, despite the fact that its consumption was continuous, for almost 3 years, and relatively evenly distributed within the years. Isbell [1990] observed a sudden short-term increase in mortality of vervet monkeys (Cercopithecus aethips) due to leopard predation in Amoseli National Park in Kenya. Isbell [1990] argued that this may have been due to an increase in the presence of the predator and an individual preference for particular prey species, perhaps as a result of earlier experience with that prey [Caro, 1980]. Predation rates have been inferred through unexplained disappearances of study animals [Peetz et al., 1992] and some studies remain skeptical about the generality of these relationships [Zuberbuhler & Jenny, 2002]. Therefore, scats analysis can give clues for assuring that predation was occurring. ACKNOWLEDGMENTS We thank O. Boticario Foundation of Nature Protection and the FACITEC for nancial support. We are grateful to Biology Museum Professor Mello Leitao for the technical support, Dr. Matt Gompper and Tadeu Gomes de Oliveira for their valuable comments and their kind help with the nal English version and Juliana Quadros for help with the techniques in the preparation of laminas. REFERENCES
Beebe W. 1925. Studies of a tropical jungle: one quarter of a square mile of jungle at Kartabo, British Guiana. Zoologica 6:1193. Bianchi RC. 2001. Estudo comparativo da dieta da jaguatirica, Leopardus pardalis (Linnaeus, 1758), em Mata Atlantica [dissertation]. Vitoria (ES): Universidade Federal do Esprito Santo. 70p. Boinski S, Treves A, Chapman CA. 2000. A critical evaluation of inuence of predators on primates: effects on group travel. In: Boinski S, Garber PA, editors. On the move: how and why animals travel in groups. Chicago: The University of Chicago Press. p 4372. Campbell CJA, Aureli F, Chapman GRF, Mathews K, Russo SE, Suarez S, Vick V. 2005. Terrestrial behavior of Ateles spp. Int J Primatol 26:10301051. Caro TM. 1980. The effects of experience on the predatory patterns of cats. Behav Neural Biol 29:128. Castro MI. 2001. RPPN Feliciano Miguel Abdalaa protected area for the northern muriqui. Neotrop Primates 9:128129. Crawshaw PG Jr. 1995. Comparative ecology of ocelot (Felis pardalis) and jaguar (Panthera onca) in a protectec subtropical forest in Brazil and Argentina [Doctoral thesis]. Florida University. 190p. Emmons LH. 1987. Comparative feeding ecology of felids in a neotropical rainforest. Behav Ecol Sociobiol 20:271283. Fonseca GAB. 1989. Small mammal species diversity in Brazilian tropical primary and secondary forests of different sizes. Rev Bras Zool 6:381422. Heymann EW. 1990. Reactions of wild Tamarins, Saguinus mystax and Saguinus fuscicollis to avian predators. Int J Primatol 11: 327337. Hisrch A. 1995. Censo de Alouatta fusca Geoffroy, 1812 (Platyrrhini, Atelidae) e qualidade do habitat em dois remanescentes de Mata Atlantica em Minas Gerais [Doctoral thesis]. Belo Horizonte (MG). Universidade Federal de Minas Gerais, 171p. Isbell LA. 1990. Sudden short-term increase in mortality of vervet monkeys (Cercopithecus aethiops) due to leopard predation in

Am. J. Primatol. DOI 10.1002/ajp

1178 / Bianchi and Mendes

Amboseli National Park, Kenya. Am J Primatol 21:4152. Karpanty SM. 2006. Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. Int J Primatol 27: 239261. Ludlow ME, Sunquist ME. 1987. Ecology and behavior of ocelots in Venezuela. Natl Geogr Res 3:447461. McGraw WS, Cooke C, Shultz S. 2006. Primates remains from African crowned eagle (Stephanoaetus coronatus) nest in Ivory Coasts Tai Forest: Implications for primate predation and early hominid taphonomy in South Africa. Am J Phys Anthropol 131:151165. Mendes SL. 1989. Estudo Ecologico de Alouatta fusca (Primates:Cebidae) na Estac ao - Biologica de Caratinga, MG. Rev Nordest Biol 6:71104. Miranda JMD, Vernardi IP, Abreu KC, Passos FC. 2005. Predation on Alouatta guariba clamitans Cabrera (Primates, Atelidae) by Leopardus pardalis (Linnaeus) (Carnivora, Felidae). Rev Bras Zool 22:793795. Miranda JMD, Bernardi IP, Moro-Rios RF, Passos FC. 2006. Antipredator behavior of brown howlers attacked by black hawkeagle in Southern Brazil. Int J Primatol 27: 10971101. Moreno RS, Kays RW, Samudio R Jr. 2006. Competitive release in diets of ocelots (Leopardus pardalis) and pumas (Puma concolor) after jaguar (Panthera onca) decline. J Mammal 87:808816. Murray L, Gardner GL. 1997. Leopardus pardalis. Mammal Species 548:110. Peetz A, Norconk MA, Kinzey WG. 1992. Predation by jaguar on howler monkey (Alouatta seniculus) in Venezuela. Am J Primatol 28:223228. Quadros J. 2002. Identicac ao microscopica - de pelos de mamferos brasileiros e sua aplica c ao no estudo da dieta de carnvoros - [Doctoral thesis]. Curitiba (PR): Universi dade Federal do Parana. 127p. Rettig NL. 1978. Breeding behavior of the harpy eagle (Harpia harpyia). Auk 95: 629643. Sanders WJ, Trapani J, Mitani JC. 2003. Taphonomic aspects of crowned hawk-eagle predation on monkeys. J Hum Evol 44: 87105. Skorupa JP. 1989. Crowned eagles Stephanoaetus coronatus in rainforest: observations on breeding chronology and diet at a nest in Uganda. Ibis 131:294298. Strier KB, Mendes SL, Santos RR. 2001. Timing of births in sympatric brown howler monkeys (Alouatta fusca clamitans) and northern muriquis (Brachyteles arachnoides hypoxanthus). Am J Primatol 55: 87100. Sunquist ME, Sunquist F. 2002. Wild cats of the world. Chicago: University of Chicago. Vasquez MRO, Heymann EW. 2001. Crested Eagle (Morphnus guianesis) predation on infant Tamarins (Saguinus mystax and Saguinus fuscicollis, Callitrichinae). Folia Primatol 72:301303. Ximenez A. 1982. Notas sobre picales VIII: observaciones sobre el contenido estomacal y el comportamiento alimentar de diversas especies de felinos. Rev Nordest Biol 5: 8991. Zuberbuhler K, Jenny D. 2002. Leopard predation and primate evolution. J Hum Evol 43:873886.

Am. J. Primatol. DOI 10.1002/ajp