Herpetology Notes, volume 11: 1069-1074 (2018) (published online on 19 December 2018)

Predation of Boana raniceps (Cope, 1862) by the common Callithrix jacchus (Linnaeus, 1758) in northeastern Brazil

Raone Beltrão-Mendes1, Francis Luiz Santos Caldas2,3, Patrício Adriano da Rocha4, and Daniel Oliveira Santana4,*

The , Callithrix jacchus (Linnaeus, between callitrichid monkey for how are 1758), is a small Neotropical (body weight caught (Stevenson and Rylands, 1988; Heymann et al., 250–400 g) endemic to the Brazilian Northeast, found in 2000; Cicchi et al., 2010). the Atlantic Forest and Caatinga (Rylands et al., 2009). The reporting of anuran predation by is This diurnal species feeds on a wide variety of foods, fundamental to the understanding that small vertebrates including fruits, leaves, plant exudates, and prey, may play a crucial role in the diet of primate species (e.g., including both invertebrates and vertebrates, in a wide Melo et al., 2018). In the present study, we report the range of habitats and under uncountable conditions predation of Boana raniceps (Cope, 1862) by a common (Rylands and Faria, 1993; Digby and Barreto, 1998; marmoset, Callithrix jacchus, in an anthropogenic Digby et al., 2011; Hilário et al., 2017). habitat in the Atlantic Forest of northeastern Brazil. , like other neotropical primates (e.g., owl The event took place in the surroundings of the monkeys, pygmy marmosets, capuchin monkeys, robust urban area of Aracaju, Sergipe State, Brazil (11.074ºS, capuchin monkeys, and ), are predators of a wide 37.121ºW; datum = WGS84; elevation ca. 4 m). The variety of small vertebrates (Freese and Oppenheimer, site is a mix of urban and rural environments, with rural 1981; Wright, 1981; Snowdon and Soini, 1988; Soini, buildings typical of farmland areas. The vegetation is 1988; Stevenson and Rylands, 1988; Kinzey, 1997; predominantly restinga, composed of both native and Amora et al., 2014), including anurans (Canale and cultivated scrubs (mango trees), with many lakes and Lingnau, 2003; Cicchi et al., 2010; Beltrão-Mendes some flooded areas. et al., 2016). The capacity for searching between live On 26 December 2012, the observer (DOS) noted a leaves, under the bark of trees, inside tree holes, along common marmoset group (at least four adult individuals) dead branches, and in bromeliads, combined with the moving and foraging, scattered in an area of about 70 seasonal differences in the environment and different m2. At around 1400 h, the marmosets started to vocalize habitat types, are decisive factors in the differences intensively after an adult grasped a treefrog, at a height of 2.1 m. The marmoset then distanced itself from the group, apparently in order to avoid sharing. While holding the by its abdomen with both hands, the marmoset started to consume it first by its head and then

1 Departamento de Ecologia, Universidade Federal de Sergipe, by eating part of its limbs (Fig. 1A–C). The marmoset Cidade Universitária, São Cristóvão, Sergipe 49100-000, also pulled out the viscera with its mouth and partially Brazil. ate them (Fig. 1D). It then released the prey, probably 2 Departamento de Biologia, Universidade Federal de Sergipe, after becoming satisfied. The remains of the frog fell to Cidade Universitária, São Cristóvão, Sergipe 49100-000, the ground, once again without any sharing with other Brazil. group members. 3 Faculdades Integradas de Sergipe, Largo Glicério Cerqueira We confirmed the frog’s identification as Boana 387, Centro, Tobias Barreto, Sergipe 35690-000, Brazil. 4 Programa de Pós-Graduação em Ciências Biológicas, raniceps by its relatively large size and its hind limbs, Universidade Federal da Paraíba, Cidade Universitária, João where dark brown to black cross-bands extended onto the Pessoa, Paraíba 58059-900, Brazil. hidden surfaces of the thighs (Fig. 2). This characteristic *Corresponding author. E-mail: [email protected] follows the descriptions by Boulenger (1889) and 1070 Raone Beltrão-Mendes et al.

Figure 1. Sequence of the predation event by Callithrix jacchus on Boana raniceps.

Figure 2. Remnants of a Chaco treefrog (Boana raniceps) partially consumed by a Common marmoset (Callithrix jacchus). Predation of Boana raniceps by the common marmoset in northeastern Brazil 1071

Table 1. Listing of reports featuring anuran predation by monkeys of the family and its respective predation fashion, prey items consumed, use of hand, season of consumption and habitat type. Only genera and species for which information is available are listed. Table 1. Listing of reports featuring anuran predation by monkeys of the family Callitrichidae and its respective predation fashion, prey items consumed, use of hand, season of consumption and habitat type. Only genera and species for which information is available are listed.

Species Prey First Limbs Trunk / When using Season Habitat References Biting Abdomen one hand Consumption Callithrix flaviceps Treefrogs - - - - Whole year Seasonal Tropical Ferrari, 1987, 1988, 1991 (higher in Rain Forest drought) Callithrix geoffroyi Frogs ------Caine, 1996 Callithrix geoffroyi Boana sp. - - - - Whole year Tropical Rain Forest Passamani and Rylands, 2000 Callithrix jacchus Frogs Head - - - Whole year Tropical Decidual Digby and Barreto, 1998 Semiarid Callithrix jacchus Scinax x-signatus - - - - Drought Tropical Rain Forest Santos, 2009 Callithrix jacchus Boana albomarginata - - - - Drought Tropical Rain Forest Santos, 2009 Callithrix jacchus Boana albomarginata Head Not - - Rainy Seasonal Tropical Beltrão-Mendes et al., observed Rain Forest 2016 Callithrix jacchus Boana raniceps Head Partially No Left Drought Seasonal Tropical present study Rain Forest Callithrix kuhli Frogs Head Yes Yes - Whole year Tropical Rain Forest Stevenson and Rylands, 1988 Callithrix kuhli Frogs - - - - Whole year Tropical Rain Forest Rylands, 1989 Callithrix penicillata Boana lundii Head Yes Yes - Drought Forested Savana Canale and Lingnau, 2003 Callithrix penicillata Treefrogs Not - - Not observed Drought Forested Savana Canale and Lingnau, 2003 observed Callithrix penicillata Boana albomarginata Head Yes Yes - Rainy Tropical Rain Forest Cicchi et al., 2010 Callithrix sp. Treefrogs - - - - Whole year Tropical Rain Forest Rangel et al., 2011 Leontopithecus caissara Frogs - - - - Drought Tropical Rain Forest Prado and Valladares- Padua, 2004 Leontopithecus chrysomelas Frogs - - - - Whole year Tropical Rain Forest Rylands, 1989 Leontopithecus chrysomelas Frogs - - - - Whole year Tropical Rain Forest Raboy and Dietz, 2004 Leontopithecus chrysopygus Frogs - - - - Whole year Seasonal Tropical Carvalho et al., 1989 Rain Forest Leontopithecus chrysopygus Treefrogs Head Yes Yes - Whole year Seasonal Tropical Passos, 1999 Rain Forest Leontopithecus chrysopygus Frogs - - - - Whole year Seasonal Tropical Passos and Keuroghlian, Rain Forest 1999; Keuroghlian and Passos, 2001 Leontopithecus chrysopygus Frogs ------Kierulff et al., 2002

Leontopithecus rosalia Frogs - - - - Whole year Tropical Rain Forest Dietz et al., 1997 Leontopithecus rosalia Frogs - - - - Whole year Tropical Rain Forest Miller and Dietz, 2006; Miller et al., 2006 Leontopithecus rosalia Frogs ------Kierulff et al., 2002 intermedius Frogs - Yes Yes - Drought Seasonal Tropical Rylands, 1979 Rain Forest Mico intermedius Frogs Head Yes Yes - Drought Seasonal Tropical Rylands, 1981 Rain Forest Mico intermedius Frogs Head Yes Yes - Drought Seasonal Tropical Stevenson and Rylands, Rain Forest 1988 Saguinus fuscicollis Frogs - - - - Whole year Tropical Rain Forest Soini, 1987 Saguinus fuscicollis Frogs - - - - Drought Seasonal Tropical Yoneda, 1984 Rain Forest Saguinus fuscicollis Frogs Head - - - Whole year Tropical Rain Forest Heymann et al., 2000 Saguinus mystax Frogs Head - - - Whole year Tropical Rain Forest Heymann et al., 2000

Duellman (1970). The Chaco treefrog, Boana raniceps, Guiana, eastern Brazil, Paraguay, northern Argentina, belongs to the B. albopuncatata group (Faivovich et al., and eastern Bolivia (Frost, 2018). Males usually call 2005; Dubois, 2017) and is the species with the greatest before sunset on higher and more distant substrates of geographical distribution of the group. Its range includes the pools, shifting at nightfall toward the water bodies the Colombian and Venezuelan Amazon, French (Guimarães and Bastos, 2003). In places close to 1072 Raone Beltrão-Mendes et al.

Table 2. Current reports on anuran predation by callitrichid primates that present any food sharing detail. Blank fields represent not reported information.

Table 2. Current reports on anuran predation by callitrichid primates that present any food sharing detail. Blank fields represent not reported information.

Callitrichid Species Individual Prey Species Sharing Discardings Group Presence Season Reference Age and Sex Size of Infants Callithrix flaviceps Adult female Treefrogs From adult - - Yes Whole year (higher Ferrari, 1987, 1991 female to infant in drought) Callithrix flaviceps - Treefrogs Not detailed - 5-15 Yes Whole year (higher Ferrari, 1988, 1991 in drought) Callithrix jacchus - Frogs None - - - Whole year Digby and Barreto, 1998 Callithrix jacchus Adult Boana albomarginata - - - - Rainy Beltrão-Mendes et al., 2016 Callithrix jacchus Adult Boana raniceps None Part of limbs; 4 Not Drought present study trunk; a small observed portion of the gut Callithrix kuhli - Frogs Not detailed - 5 No Whole year Rylands, 1989 Callithrix penicillata Subadult Boana lundii None None - Yes Drought Canale and Lingnau, 2003 male Callithrix penicillata Adult Boana albomarginata None Not detailed - - Rainy Cicchi et al., 2010 Leontopithecus - Frogs With infants, - 5-7 Yes Whole year Passos and Keuroghlian, chrysopygus but not detailed 1999; Keuroghlian and Passos, 2001 Mico intermedius - Frogs Contested by None 8-12 Yes Drought Rylands, 1981 juveniles, but not detailed Saguinus mystax - Frogs Male to Juvenile - 5 No Whole year Heymann et al 2000

them, the species usually occupy branches of shrubs or primates from New World are essentially diurnal emerging vegetation, although they also use the ground, (Kinzey, 1997; Rylands et al., 2012), whereas anurans sticks, trees, and rocks (Guimarães and Bastos, 2003; are more commonly nocturnal (Duellman and Protázio et al., 2014; Leite-Filho et al., 2015). Trueb, 1994). This temporal niche disjunction, together In the observed instance, predation occurred in the with the use of diurnal refugia and camouflage by way marmosets typically prey on anurans, by biting and anurans, likely contributes to the small representation eating the head first, followed by consumption of the of frogs in the diet of primates (Toledo et al., 2007; limbs and the rest of the body (Table 1). An intriguing Nunes and Costa, 2011). Moreover, the capturing of subject is the avoidance of prey sharing. Food sharing anurans that may be sleeping during the day depends on among callitrichids is a well-known and common the foraging and searching expertise of each individual process when infants and other group members interact (Cicchi et al., 2010). (Table 2). However, among adults, some reports Vertebrate energy intake and food sharing by describe vertebrate prey sharing as an event of high callitrichids may be intrinsically associated with, contest (see Rylands, 1981; Maier et al., 1982; Ferrari, among other factors, the hour of predation, exploited 1987; Digby and Barreto, 1998). Kleiman et al. (1988) habitat strata, preferred food item, prey size/weight, reported that lion tamarins, Leontopithecus, rarely shortage seasons, or “hostile” habitats, which present share preferred items such as vertebrate prey. This inconsistency in resource availability as xeric seemed evident during our observation when the animal environments (e.g., Kleiman et al., 1988; Digby and distanced itself far from the group, as also observed by Barreto, 1998; Heymann et al., 2000; Melo et al., Melo et al. (2018). The absence of details regarding 2018; Lüffe et al., 2018). Those isolated or combined sharing in previous reports (differences in presented ecological conditions for both the prey and predator references between Tables 1 and 2) does not allow any are reflected in the scarcity of reports (detailed or not). clear conclusion. Therefore, we advocate the reporting of further records, Most field studies on the feeding ecology of callitrichids even if anecdotal or with as much detail as possible, in show a relatively low ratio of anuran predation (Maier order to increase the understanding of the strategies of et al., 1982; Alonso and Langguth, 1989; Digby and vertebrate predation by small primates. Barreto, 1998; Passamani and Rylands, 2000; Rangel et al., 2011; Amora, 2013). Except for the genus Aotus, Predation of Boana raniceps by the common marmoset in northeastern Brazil 1073

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