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Herpetology Notes, volume 12: 833-839 (2019) (published online on 12 August 2019)

Predation on the Tropical House mabouia (: ) by the Granular Toad Rhinella major (Anura: Bufonidae), including an updated list of predation events in this of gecko

Fillipe Pedroso-Santos1, Patrick Ribeiro Sanches1, Jackson Cleiton Sousa1, and Carlos Eduardo Costa-Campos1,*

Predator-prey relationships are important ecological amphibians, , and, occasionally, rodents and bats factors in how vertebrate and invertebrate assemblages (e.g., Quiroga et al., 2009; Silva et al., 2010; Chaves et are structured (Vitt and Caldwell, 2009), altering al., 2012; Oliveira et al., 2017). utilization strategies of food resources among several species groups (Toft, 1985). In amphibians, the degree of capture specialization in terms of prey type and size changes as individuals grow (Donnelly, 1991; Simon and Toft, 1991). The increase of prey size with ontogeny may be a passive effect in some frogs (Lima et al., 2000). In , juvenile lack experience on avoiding predators (Rocha et al., 2000) and are exposed to predation by individuals of other species, but also by individuals of the same species, because their small size makes them potential prey for many predator types (e.g., Bauer, 1990; Siqueira and Rocha, 2008). Predation therefore represents an important factor in regulating populations (Siqueira and Rocha, 2008). Rhinella major (Müller and Hellmich, 1936) is a terrestrial toad and a member of the R. granulosa group. Adults are of moderate size (35.8–72.8 mm in males and 33.9–81.1 mm in females; Narvaes and Rodrigues, 2009) and the species occurs in open habitat in the Chaco region of Bolivia, Paraguay, Argentina, and Brazilian Amazonia (Frost, 2017). Toads of the Rhinella Fitzinger, 1826 are considered generalist predators (e.g., Moseley et al., 2005) and are known to feed on arthropods, but they may also ingest plant parts (e.g., pieces of leaves) and vertebrates such as

Figure 1. Predation of a juvenile Hemidactylus mabouia by an adult female Rhinella major observed in Macapá 1 Universidade Federal do Amapá, Departamento de Ciências Municipality, Amapá State, Brazil. (A) Rhinella major with Biológicas e da Saúde, Laboratório de Herpetologia, Macapá, prey in its mouth. (B) Dorsal views of the specimens, with the Amapá 68903-419, Brazil. partly digested H. mabouia removed from the stomach of the * Corresponding author. E-mail: [email protected] toad. Photos by Fillipe Pedroso dos Santos. 834 Fillipe Pedroso-Santos et al.

The , Hemidactylus mabouia Results (Moreau de Jonnès, 1818), is a medium-sized lizard Our field observations indicate that the ingestion of (maximum 67.9 mm in males; Kluge, 1969) introduced the juvenile lizard must have started headfirst, for at the from into the tropics of , Central time of observation only the posterior dorsal portion America, and the (Butterfield et al., 1993; of its body was visible (Fig. 1A). The adult R. major Carranza and Arnold, 2006; Henderson and Powell, moved a distance of about 4 m away from the initial 2009). This gecko presents nocturnal habits and can observation site with the prey in its mouth. It did not be found in several Brazilian ecosystems, mainly in regurgitate the prey. The entire event lasted ca. 15 min. anthropic environments, and it is considered an invasive After the successful predation event, the toad remained exotic species in Brazil (Vanzolini, 1978; Anjos and motionless for 10 min. Rocha, 2008; Rocha et al., 2011). In the area of the During the dissection of the toad, we were able to present study, H. mabouia is sympatric with R. major. determine that it was an adult female (SVL = 45 mm; We here report for the first time the predation on H. body weight 8 g). Based on its overall morphology mabouia by R. major and present a list of predation (Powell et al., 1998), the prey was identified as a juvenile records for H. mabouia. H. mabouia (SVL = 25 mm; total length = 40 mm; Fig. 1B), which distended the toad’s stomach. Materials and Methods Other authors have reported H. mabouia as a prey The predation event was observed on 2 November 2017 species of amphibians, birds, lizards, snakes, and at around 21:30 h, during an amphibian survey in an (Vitt et al., 1996; Faria and Araújo, 2004; urban area in the municipality of Macapá, Amapá State, Passos et al., 2016). We have compiled a list of these Brazil (0.0083ºS, 51.0953ºW; WGS84; elevation 7 m). predation events (Table 1) by accessing primarily The toad was sacrificed with anaesthetic (2% lidocaine); papers published in the journals Herpetological Review the gecko had been killed in the interaction. Voucher and Herpetology Notes as well as via Internet searches specimens were fixed in 10% formalin, preserved in 70% using the keywords “predation,” “gekkonid lizards,” ethanol, and deposited in the Herpetological Collection and “tropical house gecko.” We recovered a total of 54 of Universidade Federal do Amapá (Carlos Eduardo reported predation events involving H. mabouia as prey Costa-Campos field number CECCAMPOS 0946 for (Table 1). The most frequent predators were snakes (29 R. major, CECCAMPOS 0947 for H. mabouia). Body species), followed by lizards (6), birds (3), spiders (3), length (snout–vent length, SVL) was measured with amphibians (1) and mammals (1). Overall, only four Mitutoyo digital callipers to the nearest mm and mass cases presented cannibalistic H. mabouia predation. was obtained using a manual Pesola balance to the In summary, our findings suggest that H. mabouia nearest gram. The toad’s stomach was excised between may represent a potential prey for Rhinella major and the cardiac and pyloric sphincters, and stomach contents other species, especially in urban areas. In addition, the were analysed under a Zeiss Stemi 2000-C stereoscopic updated list presented in this study may be useful for microscope. In addition, in this study we updated the list guiding future studies on the feeding ecology of these provided by Nogueira et al. (2013), adding new species predators, their prey, and the food webs in which they as predators of H. mabouia. interact.

Table 1. Updated list of Hemidactylus mabouia predators, revised and adapted based on the list published by Nogueira et al. (2013).

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Family/species Source FROGS Predation onBufonidae the Tropical (1) House Gecko by the Granular Toad 835 Rhinella major (Müller and Hellmich, 1936) this paper Table 1. Continued.Hylidae (1) Scinax x-signatus (Spix, 1824) Zanchi-Silva and Borges-Nojosa (2017) Family/species Source BIRDS Accipitridae (1) Rupornis magnirostris (Gmelin, 1788) De Macêdo and Freire (2010) Cuculidae (2) Crotophaga ani Linnaeus, 1758 Figueiredo-de-Andrade and Silveira (2012) Guira guira (Gmelin, 1788) Andrade et al. (2015)

LIZARDS (1) Anolis leachii (Duméril and Bibron, 1837) Trageser et al. (2018) Gekkonidae (1) Hemidactylus mabouia (Moreau de Jonnès, 1818) Zamprogno and Teixeira (1998); Pombal and Pombal-Jr. (2010); Costa-Campos and Furtado (2013); Lyakurwa (2017) Leiosauridae (1) Enyalius perditus Jackson, 1978 Muscat et al. (2016) Scincidae (1) Mabuya agilis (Raddi, 1823) Vrcibradic and Rocha (2002) Teiidae (1) Cnemidophorus littoralis Rocha et al., 2000 Menezes et al. (2006) Tropiduridae (1) Tropidurus torquatus (Wied-Neuwied, 1820) Araújo (1991); Rocha and Vrcibradic (1998); Teixeira and Giovanelli (1999); Galdino and Van Sluys (2004)

MAMMALS Callitrichidae (1) Callithrix penicillata (Geoffroy, 1812) Rocha-Santos et al. (2013)

SNAKES Boidae (1) Chilabothrus chrysogaster chrysogaster (Cope, 1871) Reynolds et al. (2017) (7) Borikenophis portoricensis (Reinhardt and Lütken, 1862) Grant (1932); Henderson and Sajdak (1996) Chironius exoletus (Linnaeus, 1758) Rodrigues (2007) Chironius bicarinatus (Wied-Neuwied, 1820) Vrcibradic and Eisfeld (2016) Leptophis ahaetulla (Linnaeus, 1758) De Albuquerque et al. (2007); Germano and França, (2017) Leptophis depressirostris (Cope, 1861) Thomas (1976) Oxybelis fulgidus (Daudin, 1803) Santos-Jr. et al. (2011) Oxybelis aeneus (Wagler, 1824) Franzini et al. (2018) Dipsadidae (17) Caaeteboia amarali (Wettstein, 1930) Passos et al. (2012) Erythrolamprus typhlus (Linnaeus, 1758) Da Silva et al. (2010) Leptodeira annulata (Linnaeus, 1758) Cantor and Pizzatto (2008) Family/species Source Lygophis flavifrenatus (Cope, 1862) De Lema et al. (1983); Michaud and Dixon (1989) Oxyrhopus clathratus Duméril et al., 1854 Morato (2005) Oxyrhopus guibei Hoge and Romano, 1978 Rocha and Vrcibradic (1998); Barbo (2008); Barbo et al. (2011) Oxyrhopus petolarius (Linnaeus, 1758) Nogueira et al. (2013) Oxyrhopus trigeminus Duméril et al., 1854 Alencar et al. (2012) Philodryas nattereri Steindachner, 1870 De Mesquita et al. (2011) Philodryas olfersii (Liechtenstein, 1823) Thomas (1976) Phylodryas patogoniensis (Girard, 1858) Barbo et al. (2011) Siphlophis pulcher (Raddi, 1820) Sazima and Argôlo (1994) Siphlophis worontzowi (Prado, 1940) Bernarde and Abe (2010) Thamnodynastes pallidus (Linnaeus, 1758) Rocha and Vrcibradic (1998) Thamnodynastes strigatus (Günther, 1858) Bernarde et al. (2000) Tropidodryas serra (Schlegel, 1837) De Oliveira (2008) Tropidodryas striaticeps (Cope, 1870) De Oliveira (2008) Elapidae (1) Micrurus frontalis (Duméril et al., 1854) De Lema et al. (1983) Viperidae (3) Bothrops alcatraz Marques et al., 2002 Marques et al. (2002) Bothrops insularis (Amaral, 1922) Duarte et al. (1995) Bothrops jararaca (Wied-Neuwied, 1824) Sazima (1992); Barbo (2008); Barbo et al. (2011)

SPIDERS Ctenidae (1) Unidentified ctenid Lanschi and Ferreira (2012) Lycosidae (1) Unidentified lycosid spider Koski et al. (2013) 836 Fillipe Pedroso-Santos et al.

Table 1. Continued.

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Accepted by Hinrich Kaiser