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A uniao faz a forca: observacao de cachorros-do-mato (Cerdocyon thous) cooperativamente predando seu potencial predador.

STRONGER TOGETHER: OBSERVATION ON CRABEATING FOXES (Cerdocyon thous) COOPERATIVELY PREYING THEIR POTENTIAL PREDATOR

The crab-eating fox, Cerdocyon thous (Linnaeus, 1766), is a nocturnal, medium-sized canid (5-8 kg), with a wide distribution across South America (Berta 1982; Sillero-Zubiri 2009). It occurs in a range of habitats, including marshlands, savannahs, scrublands, forests, and human-altered areas (Courtenay & Maffei 2004; Beisiegel et al. 2013). Crab-eating foxes are opportunistic feeders that consume a variety of fruits, invertebrates, and small vertebrates, and may shift their diet seasonally (e.g., Facure et al. 2003; Gatti et al. 2006; Pedo et al. 2006; Lemos et al. 2011; Bianchi et al. 2014; Dias & Bocchiglieri 2015). However, most of the species feeding ecology is known from scat analysis, although this method alone does not address all different aspects of feeding behavior (Zabala & Zuberogoitia 2003; Klare et al. 2011). Observational studies have much to contribute to the current knowledge of feeding and social habits of the crab-eating fox and other carnivores.

Crab-eating foxes are monogamous, with moderate and flexible social behavior (Biben 1982). Although commonly seen in pairs or small family groups (Montgomery & Lubin 1978; Brady 1979; Macdonald & Courtenay 1996; Lemos et al. 2011), they are considered solitary hunters and normally each individual in a pair captures and consumes its own food (Brady 1979), which consist on fruits and small preys (e.g., invertebrates, rodents, and birds). This supports the general rule that relates prey mass to carnivore foraging group size (Moehlman 1989). However, crab-eating foxes forage close to each other and may tolerate the presence of conspecifics during ingestion of abundant food items (e.g., when preying on Squamata and Testudines eggs, or scavenging carcasses of large animals; Montgomery & Lubin 1978; Brady 1979; Facure et al. 2003; Courtenay & Maffei 2004; Lemos et al. 2011). Presumably, such tolerance could allow individuals of a group to benefit from shared resources. In this aspect, little is known about predation upon large preys by South American canids and the potential role of social interactions in these events. Recently, Chatellenaz & Guzman (2015) described a predation event by two Pampas foxes, Lycalopex gymnocercus (G. Fischer, 1814), on an adult of South American brown brocket, Mazama gouazoubira (G. Fischer [von Waldheim], 1814), in Argentina, suggesting it as a rare and unusual event for South American canid species. Here, we describe the first record of a cooperative attack by two crab-eating foxes upon a live adult short-tailed boa, Boa constrictor amarali (Stull, 1932), reporting its consumption by this South American canid.

Boa constrictor amarali is a large-bodied snake with mean length of 144 cm and mean weight of 3.5 kg (0.1-6.09 kg, N = 53) (Cutolo et al. 2012). It has a wide distribution ranging from eastern Bolivia to Brazilian southern states (Hynkova et al. 2009). Previous studies have reported boas ingesting several medium-sized mammals (Perry et al. 2002; Ferrari et al. 2004; Quintino & Bicca-Marques 2013), including some medium-sized carnivores such as an adult jaguarundi, Puma yagouaroundi (E. Geoffroy, 1803) (Monroy-Vilchis et al. 2011), dwarf coatis, Nasua nelsoni (Merriam, 1901), Cozumel raccoons, Procyon pygmaeus (Merriam, 1901) (McFadden et al. 2010), kinkajous, Potos flavus (Schreber, 1774) (Sunyer & Galindo-Uribe 2015), and also a failed attempt upon a crab-eating fox (Almiron et al. 2011).

Our opportunistic observation of a pair of crab-eating foxes attacking and killing an adult short-tailed boa was made on September 2006 (Fig. S1). The interaction lasted about 20 minutes and happened at the end of the afternoon (ca.18:30 h), at an anthropized remnant of Cerrado, near MS-178 highway (20[degrees]58' 10.85" S /56[degrees]31'05.78" W), at the municipality of Bonito, Mato Grosso do Sul State, Brazil. The observation was filmed and photographed from a distance that did not influence the behavior of the animals. When first sighted, crab-eating foxes were already attacking the boa. Therefore, we do not know details on how the interaction started. However, it was possible to observe that the short-tailed boa was alive and actively trying to defend itself, curling up and striking back against the crab-eating foxes. No signs of crab-eating foxes' den or litter were detected within 100 m of the site of interaction spot. No clues of defensive (parental) behavior (e.g., threaten and alert or siren calls) of the types reported for crab-eating foxes (Brady 1979, 1981; Lemos & Azevedo unpublished data) and other South American canids (Chatellenaz et al. 2018) were detected. This apparent lack of parental behavior reinforces the notion that this was a predatory, not defensive behavior.

During the whole observation crab-eating foxes acted jointly and cooperatively. Attacks consisted of alternate or simultaneous bites by the two crab-eating foxes to the short-tailed boa, followed by several jolts and strong pulls in opposite directions. The short-tailed boa constantly wrapped itself in order to protect its head, suggesting a defensive behavior. Joint attacks prevented an effective defense response by the boa, making it vulnerable against its attackers. After several bites, the boa started to show evident apathy and the crab-eating foxes signs of tiredness. Then the crab-eating foxes took turns on the attacking, while the other rested at the side. A lethal neck-bite killed the snake, which remained stretched, belly up, motionless on the ground. With the natural daylight gone, it was not possible to carry observations on the total ingestion of the prey. However, after the death of the boa, the female crab-eating fox started growling at the male when the latter approached the snake, displaying a behavior that may indicate a sign of dominance and a sort of hierarchy during prey consumption.

Although C. thous is frequently observed foraging in pairs but not sharing resources most of the time (Brady 1979; Lemos & Facure 2011), the two crab-eating foxes displayed elaborated sociality and an ability to kill a prey cooperatively. Similar cooperative behavior for subjugating larger prey has been reported for bush dogs, Speothos venaticus (Lund, 1842), a highly social canid that may live and hunt in groups of up to 12 individuals (Beisiegel & Ades 2002; Lima et al. 2012). Apparently, the uninterrupted attack to the boa, through several and alternating bites by both members of the pair, was an important strategy to successfully subjugate the snake, preventing effective defense.

Records of cooperative hunting on large preys for C. thous are virtually nonexistent to our knowledge, except for one single description by R. Rudran at Brady (1979), who reports an ambush of a tegu (Tupinambis sp.) by a pair of crab-eating foxes. At the occasion the canids displayed similar behaviors of alternating at repeatedly attacking the prey, followed by pulling it in opposite directions and, finally, growling to each other once the prey was killed. Our new record, combined with those of Brady (1979) and Chatellenaz & Guzman (2015), suggests that the benefits of sharing food may occasionally drive species away from the general rule predicted for small canids (Moehlman 1989). Additionally, the observation indicates that crab-eating foxes may actually prey on snakes (Gonzalez et al. 2016), instead of only ingesting them through scavenging (Rocha et al. 2004). Boas are not only a large prey but also a potential crab-eating fox predator (Almiron et al. 2011). Therefore, our record opens the possibility that pairs of crab-eating foxes may consume other large preys, including some found in scats that are generally considered as carcass intake.

Considering the lack of observational records on feeding behavior for South American canids, our report is an important contribution for the current knowledge on the feeding ecology and hunting strategy for this group. We recommend the development of natural history studies associating direct observation to other methods (e.g., Global Positional System monitoring) for better understanding social relationships and interspecific interactions that may shape behavioral habits of South American canids.

https://doi.org/10.31687/saremMN.18.25.2.0.13

Acknowledgments. We are grateful to Dr. Alan N. Costa, Daniel G. Rocha, Dr. Katia G. F. Giaretta, Mozart C. Freitas-Junior and an anonymous reviewer for suggestions on earlier versions of the manuscript.

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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.

Marina X. da Silva (1), Apolonio N. S. Rodrigues (2), Fernanda C. Azevedo (3,4) and Frederico G. Lemos (3,4)

(1) Independent scholar, Foz do Iguacu, PR, Brazil. [Correspondence: Marina X. da Silva <xavier.marina@gmail.com>]

(2) Instituto Chico Mendes de Conservacao da Biodiversidade, Foz do Iguacu, PR, Brazil.

(3) Programa de Conservacao Mamiferos do Cerrado--PCMC, Cumari, GO, Brazil.

(4) Departamento de Ciencias Biologicas, Universidade Federal de Goias/Regional Catalao, Catalao, GO, Brasil.
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Author:da Silva, Marina X.; Rodrigues, Apolonio N.S.; Azevedo, Fernanda C.; Lemos, Frederico G.
Publication:Mastozoologia Neotropical
Date:Dec 1, 2018
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