Mastozoología Neotropical ISSN: 0327-9383 ISSN: 1666-0536 [email protected] Sociedad Argentina para el Estudio de los Mamíferos Argentina
da Silva, Marina X.; Rodrigues, Apolonio N. S.; Azevedo, Fernanda C.; Lemos, Frederico G. STRONGER TOGETHER: OBSERVATION ON CRABEATING FOXES (Cerdocyon thous) COOPERATIVELY PREYING THEIR POTENTIAL PREDATOR Mastozoología Neotropical, vol. 25, no. 2, 2018, July-December, pp. 499-503 Sociedad Argentina para el Estudio de los Mamíferos Argentina
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Nota
STRONGER TOGETHER: OBSERVATION ON CRAB- EATING FOXES (Cerdocyon thous) COOPERATIVELY PREYING THEIR POTENTIAL PREDATOR
Marina X. da Silva1, Apolonio N. S. Rodrigues2, Fernanda C. Azevedo3, 4 and Frederico G. Lemos3, 4
1 Independent scholar, Foz do Iguaçu, PR, Brazil. [Correspondence: Marina X. da Silva
ABSTRACT. We describe the first record of cooperative predation by two crab-eating foxes Cerdocyon( thous) upon an adult short-tailed boa (Boa constrictor amarali) at a Brazilian Cerrado spot. Although it is known that C. thous forages in pairs or in small family groups, there has been no report of crab-eating foxes preying coop- eratively on medium and large-sized preys until now. Our observation sheds light on a poorly-known aspect of feeding behavior of C. thous that could not be recorded through scat analysis, which is currently main source of information on carnivores’ feeding ecology.
RESUMO. A união faz a força: observação de cachorros-do-mato (Cerdocyon thous) cooperativamente pre- dando seu potencial predador. Descrevemos o primeiro registro de predação cooperativa por dois cachorros-do- -mato (Cerdocyon thous) sobre uma jibóia adulta (Boa constrictor amarali) em um ponto do Cerrado brasileiro. Embora seja conhecido que cachorros-do-mato forrageiem em pares ou pequenos grupos familiares, não existem até o momento registros de cachorros-do-mato cooperativamente predando presas de médio e grande porte. Nossa observação lança luz sobre um aspecto pouco conhecido do comportamento alimentar de C. thous que não poderia ser registrado por análise de fezes, principal fonte atual de informações sobre ecologia alimentar de carnívoros.
Key words: Boa constrictor, Carnivora, feeding ecology, social behavior, South American canids.
Palavras chave: Boa constrictor, canídeos sulamericanos, Carnivora, comportamento social, ecologia alimentar.
The crab-eating fox, Cerdocyon thous (Lin- and human-altered areas (Courtenay & Maffei naeus, 1766), is a nocturnal, medium-sized 2004; Beisiegel et al. 2013). Crab-eating foxes canid (5-8 kg), with a wide distribution across are opportunistic feeders that consume a variety South America (Berta 1982; Sillero-Zubiri of fruits, invertebrates, and small vertebrates, 2009). It occurs in a range of habitats, includ- and may shift their diet seasonally (e.g., Facure ing marshlands, savannahs, scrublands, forests, et al. 2003; Gatti et al. 2006; Pedó et al. 2006;
Recibido 5 abril 2018. Aceptado 12 junio 2018. Editor asociado: M. Weber 500 Mastozoología Neotropical, 25(2):499-503, Mendoza, 2018 M. X. da Silva et al. http://www.sarem.org.ar - http://www.sbmz.com.br
Lemos et al. 2011; Bianchi et al. 2014; Dias et al. 2012). It has a wide distribution ranging & Bocchiglieri 2015). However, most of the from eastern Bolivia to Brazilian southern states species feeding ecology is known from scat (Hynková et al. 2009). Previous studies have analysis, although this method alone does not reported boas ingesting several medium-sized address all different aspects of feeding behav- mammals (Perry et al. 2002; Ferrari et al. 2004; ior (Zabala & Zuberogoitia 2003; Klare et al. Quintino & Bicca-Marques 2013), including 2011). Observational studies have much to some medium-sized carnivores such as an adult contribute to the current knowledge of feeding jaguarundi, Puma yagouaroundi (É. Geoffroy, and social habits of the crab-eating fox and 1803) (Monroy-Vilchis et al. 2011), dwarf coa- other carnivores. tis, Nasua nelsoni (Merriam, 1901), Cozumel Crab-eating foxes are monogamous, with raccoons, Procyon pygmaeus (Merriam, 1901) moderate and flexible social behavior (Biben (McFadden et al. 2010), kinkajous, Potos flavus 1982). Although commonly seen in pairs or (Schreber, 1774) (Sunyer & Galindo-Uribe small family groups (Montgomery & Lubin 2015), and also a failed attempt upon a crab- 1978; Brady 1979; Macdonald & Courtenay eating fox (Almiron et al. 2011). 1996; Lemos et al. 2011), they are considered Our opportunistic observation of a pair solitary hunters and normally each individual of crab-eating foxes attacking and killing an in a pair captures and consumes its own food adult short-tailed boa was made on September (Brady 1979), which consist on fruits and small 2006 (Fig. S1). The interaction lasted about preys (e.g., invertebrates, rodents, and birds). 20 minutes and happened at the end of the This supports the general rule that relates afternoon (ca.18:30 h), at an anthropized rem- prey mass to carnivore foraging group size nant of Cerrado, near MS-178 highway (20°58′ (Moehlman 1989). However, crab-eating foxes 10.85″ S /56°31′05.78″ W), at the municipality of forage close to each other and may tolerate Bonito, Mato Grosso do Sul State, Brazil. The the presence of conspecifics during ingestion observation was filmed and photographed from of abundant food items (e.g., when preying on a distance that did not influence the behavior Squamata and Testudines eggs, or scavenging of the animals. When first sighted, crab-eating carcasses of large animals; Montgomery & foxes were already attacking the boa. Therefore, Lubin 1978; Brady 1979; Facure et al. 2003; we do not know details on how the interaction Courtenay & Maffei 2004; Lemos et al. 2011). started. However, it was possible to observe Presumably, such tolerance could allow individ- that the short-tailed boa was alive and actively uals of a group to benefit from shared resources. trying to defend itself, curling up and striking In this aspect, little is known about predation back against the crab-eating foxes. No signs of upon large preys by South American canids crab-eating foxes’ den or litter were detected and the potential role of social interactions in within 100 m of the site of interaction spot. these events. Recently, Chatellenaz & Guzmán No clues of defensive (parental) behavior (e.g., (2015) described a predation event by two Pam- threaten and alert or siren calls) of the types pas foxes, Lycalopex gymnocercus (G. Fischer, reported for crab-eating foxes (Brady 1979, 1814), on an adult of South American brown 1981; Lemos & Azevedo unpublished data) and brocket, Mazama gouazoubira (G. Fischer [von other South American canids (Chatellenaz et Waldheim], 1814), in Argentina, suggesting it as al. 2018) were detected. This apparent lack of a rare and unusual event for South American parental behavior reinforces the notion that canid species. Here, we describe the first re- this was a predatory, not defensive behavior. cord of a cooperative attack by two crab-eating During the whole observation crab-eating foxes upon a live adult short-tailed boa, Boa foxes acted jointly and cooperatively. Attacks constrictor amarali (Stull, 1932), reporting its consisted of alternate or simultaneous bites by consumption by this South American canid. the two crab-eating foxes to the short-tailed Boa constrictor amarali is a large-bodied boa, followed by several jolts and strong pulls snake with mean length of 144 cm and mean in opposite directions. The short-tailed boa weight of 3.5 kg (0.1-6.09 kg, N = 53) (Cutolo constantly wrapped itself in order to protect CRAB-EATING FOXES COOPERATIVELY PREYING THEIR POTENTIAL PREDATOR 501 its head, suggesting a defensive behavior. Joint crab-eating foxes may actually prey on snakes attacks prevented an effective defense response (Gonzalez et al. 2016), instead of only ingest- by the boa, making it vulnerable against its ing them through scavenging (Rocha et al. attackers. After several bites, the boa started 2004). Boas are not only a large prey but also to show evident apathy and the crab-eating a potential crab-eating fox predator (Almiron foxes signs of tiredness. Then the crab-eating et al. 2011). Therefore, our record opens the foxes took turns on the attacking, while the possibility that pairs of crab-eating foxes may other rested at the side. A lethal neck-bite consume other large preys, including some killed the snake, which remained stretched, found in scats that are generally considered belly up, motionless on the ground. With the as carcass intake. natural daylight gone, it was not possible to Considering the lack of observational records carry observations on the total ingestion of on feeding behavior for South American canids, the prey. However, after the death of the boa, our report is an important contribution for the the female crab-eating fox started growling at current knowledge on the feeding ecology and the male when the latter approached the snake, hunting strategy for this group. We recommend displaying a behavior that may indicate a sign the development of natural history studies as- of dominance and a sort of hierarchy during sociating direct observation to other methods prey consumption. (e.g., Global Positional System monitoring) Although C. thous is frequently observed for better understanding social relationships foraging in pairs but not sharing resources and interspecific interactions that may shape most of the time (Brady 1979; Lemos & Facure behavioral habits of South American canids. 2011), the two crab-eating foxes displayed elaborated sociality and an ability to kill a prey Acknowledgments. We are grateful to Dr. Alan N. Costa, cooperatively. Similar cooperative behavior for Daniel G. Rocha, Dr. Kátia G. F. Giaretta, Mozart C. Freitas-Junior and an anonymous reviewer for suggestions subjugating larger prey has been reported for on earlier versions of the manuscript. bush dogs, Speothos venaticus (Lund, 1842), a highly social canid that may live and hunt LITERATURE CITED in groups of up to 12 individuals (Beisiegel Almiron, D., H. Hulsberg, N. Luna, & T. Waller. & Ades 2002; Lima et al. 2012). Apparently, 2011. A failed swallowing attempt upon a crab-eating the uninterrupted attack to the boa, through fox (Cerdocyon thous Hamilton-Smith, 1839) by the several and alternating bites by both mem- Argentine Boa constrictor (Boa constrictor occidentalis bers of the pair, was an important strategy to [Philippi , 1873 ]). Herpetology Notes 4:359-362. Beisiegel, B. M., & C. Ades. 2002. The behavior of the successfully subjugate the snake, preventing bush dog (Speothos venaticus Lund, 1842) in the field: effective defense. a review. Revista de Etologia 4:17-23. Records of cooperative hunting on large preys Beisiegel, B. M., F. G. Lemos, F. C. Azevedo, D. Queirolo, for C. thous are virtually nonexistent to our & R. S. P. Jorge. 2013. Avaliação do risco de extinção do cachorro-do-mato Cerdocyon thous (Linnaeus, knowledge, except for one single description 1766) no Brasil. Biodiversidade Brasileira 3:138-145. by R. Rudran at Brady (1979), who reports an Berta, A. 1982. Cerdocyon thous. Mammalian Species ambush of a tegu (Tupinambis sp.) by a pair of 186:1-4. crab-eating foxes. At the occasion the canids Bianchi, R. C., R. C. Campos, N. L. Xavier-Filho, N. Olifiers, M. E. Gompper, & G. Mourão. 2014. displayed similar behaviors of alternating at re- Intraspecific, interspecific, and seasonal differences peatedly attacking the prey, followed by pulling in the diet of three mid-sized carnivores in a large it in opposite directions and, finally, growling to Neotropical wetland. Acta Theriologica 59:13-23. each other once the prey was killed. Our new Biben, M. 1982. Ontogeny of social behaviour related to feeding in the crab-eating fox (Cerdocyon thous) record, combined with those of Brady (1979) and the bush dog (Speothos venaticus). Journal of and Chatellenaz & Guzmán (2015), suggests Zoology 52:23-30. that the benefits of sharing food may occasion- Brady, C. A. 1979. Observation on the behavior and ally drive species away from the general rule ecology of the crab-eating fox (Cerdocyon thous). Vertebrate ecology in the northern Neotropics predicted for small canids (Moehlman 1989). (J. F. Eisenberg, ed.). Smithsonian Institute Press, Additionally, the observation indicates that Washingtom. 502 Mastozoología Neotropical, 25(2):499-503, Mendoza, 2018 M. X. da Silva et al. http://www.sarem.org.ar - http://www.sbmz.com.br
Brady, C. A. 1981. The vocal repertoires of the bush dog Lemos, F. G., K. G. Facure, & F. C. Azevedo. 2011. A first (Speothos venaticus), crab-eating fox (Cerdocyon thous), approach to the comparative ecology of the hoary fox and maned wolf (Chrysocyon brachyurus). Animal and the crab-eating fox in a fragmented human altered Behaviour 29:649-669. landscape in the Cerrado biome at Central Brazil. Chatellenaz, M. L., & A. E. Guzmán [online]. 2015. Middle-Sized Carnivores in Agricultural Landscapes Predation on a brown brocket by pampas foxes. Canid (L. M. Rosalino & C. Gheler-Costa, eds.). Nova Science Biology & Conservation 18:1-2. Publishers, New York. Chatellenaz, M. L., G. C. Müller, & G. A. Vallejos Lima, E. S. et al. 2012. First telemetry study of bush dogs: [online]. 2018. Pampas foxes as prey of yellow home range, activity and habitat selection. Wildlife anacondas. Canid Biology & Conservation 21:1-3. Research 39:512-519. Courtenay, O., & L. Maffei. 2004. Crab-eating Macdonald, D. W., & O. Courtenay. 1996. Enduring fox Cerdocyon thous (Linnaeus, 1776). Canids: social relationships in a population of crab-eating Foxes, Wolves, Jackals and Dogs (C. Sillero-Zubiri, zorros, Cerdocyon thous, in Amazonian Brazil M. Hoffmann & D. W. Macdonald, eds.). IUCN/SSC (Carnivora, Canidae). Journal of Zoology 239:329-355. Canid Specialist Group press, Gland, Switzerland and Mcfadden, K. W., D. García-Vasco, A. D. Cuarón, Cambridge, UK. D. Valenzuela-Galván, R. A. Medellín, & M. E. Cutolo, A. A., A. K. M. Teodoro, & P. M. Junior. 2012. Gompper. 2010. Vulnerable island carnivores: the Absence of ectoparasites in Boa constrictor amarali endangered endemic dwarf procyonids from Cozumel (Squamata: Boidae) from anthropic environments of Island. Biodiversity and Conservation 19:491-502. the Capivari River Basin, São Paulo state, Brazil. Acta Moehlman, P. D. 1989. Intraspecific variation in canid Veterinaria Brasilica 6:219-222. social systems. Carnivore, Behavior, Ecology and Dias, D. M., & A. Bocchiglieri. 2015. Trophic and spatio- Evolution (J. L. Gittleman, ed.). Cornell University temporal niche of the crab-eating fox, Cerdocyon thous Press, Ithaca, USA. (Linnaeus, 1766) (Carnivora: Canidae), in a remnant Monroy-Vilchis, O., Ó. Sánchez, & V. Urios. 2011. of the Caatinga in northeastern Brazil. Mammalia Consumption of an adult Puma yagouaroundi (Felidae) 80:281-291. by the snake Boa constrictor (Boidae) in Central Facure, K. G., A. A. Giaretta, & E. L. A. Monteiro- Mexico. Revista Mexicana de Biodiversidad 82:319-321. Filho. 2003. Food habits of the crab-eating fox, Montgomery, G. G., & Y. D. Lubin. 1978. Social structure Cerdocyon thous, in an altitudinal forest of the and food habits of crab-eating fox (Cerdocyon thous) Mantiqueira Range, southeastern Brazil. Mammalia in Venezuelan llanos. Acta Cientifica Venezolana 67:503-511. 29:392-393. Ferrari, S. F., W. L. A. Pereira, R. R. Santos, & L. M. Pedó, E., A. C. Tomazzoni, S. M. Hartz, & A. U. Veiga. 2004. Fatal attack of a Boa constrictor on Christoff. 2006. Diet of crab-eating fox, Cerdocyon a bearded saki (Chiropotes satanas utahicki). Folia thous (Linnaeus) (Carnivora, Canidae), in a suburban Primatologica 75:111-113. area of southern Brazil. Revista Brasileira de Zoologia Gatti, A., R. Bianchi, C. R. X. Rosa, & S. L. Mendes. 23:637-641. 2006. Diet of the crab-eating fox, Cerdocyon thous Perry, S., J. H. Manson, G. Dower, & E. Wikberg. (Carnivora, Canidae) in Paulo Cesar Vinha State 2002. White-faced capuchins cooperate to rescue a Park, Espírito Santo State, Brazil. Mammalia groupmate from a Boa constrictor. Folia Primatologica 70:153-155. 74:109-111. Gonzalez, R. C., T. M. Castro, & T. Silva-Soares. Quintino, E. P., & J. C. Bicca-Marques. 2013. Predation 2016. Predation of the water snake Erythrolamprus of Alouatta puruensis by Boa constrictor. Primates miliaris (Serpentes: Dipsadidae) by the crab-eating 54:325-330. fox Cerdocyon thous (Carnivora: Canidae). Boletim do Rocha, V. J., N. R. Reis, & M. L. Sekiama. 2004. Dieta e Museu de Biologia Mello Leitão 38:315-323. dispersão de sementes por Cerdocyon thous (Linnaeus) Hynková, I., Z. Starostová, & D. Frynta. 2009. (Carnivora, Canidae), em um fragmento florestal Mitochondrial DNA variation reveals recent no Paraná, Brasil. Revista Brasileira de Zoologia evolutionary history of main boa constrictor clades. 21:871-876. Zoological Science 26:623-631. Sillero-Zubiri, C. 2009. Family Canidae (dogs). Klare, U., J. F. Kamler, & D. W. Macdonald. 2011. Handbook of the mammals of the world (D. E. Wilson A comparison and critique of different scat-analysis & R. A. Mittermeier, eds.). Lynx Edicions, Barcelona. methods for determining carnivore diet. Mammal Sunyer, J., & D. M. Galindo-Uribe. 2015. Boa constrictor Review 41:294-312. (Boa Constrictor). Diet. Herpetological Review 46:100. Lemos, F. G., & K. G. Facure. 2011. Seasonal variation in Zabala, J., & I. Zuberogoitia. 2003. Badger, Meles foraging group size of crab-eating foxes and hoary foxes meles (Mustelidae, Carnivora), diet assessed through in the Cerrado biome, Central Brazil. Mastozoología scat-analysis: a comparison and critique of different Neotropical 18:239-245. methods. Folia Zoologica 52:23-30. CRAB-EATING FOXES COOPERATIVELY PREYING THEIR POTENTIAL PREDATOR 503
SUPPLEMENTARY ONLINE MATERIAL Supplement 1 https://www.sarem.org.ar/wp-content/uploads/2018/11/SAREM_MastNeotrop_25-2_Silva-sup1.wmv Fig. S1. Video record of crab-eating foxes (Cerdocyon thous) cooperatively subjugating an adult of short-tailed boa (Boa constrictor amarali) in Bonito, Mato Grosso do Sul state, Brazil.