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Herpetology Notes, volume 12: 869-872 (2019) (published online on 14 August 2019)

Necrophagy on granulosa (Amphibia, Anura, Bufonidae) by the aquatic families Hydrophilidae and (Insecta, Coleoptera) in Caatinga environment, Northeastern Brazil

Thiago Silva-Soares1,*, Juliana Lopes Segadilha2, Rafael B. Braga3, and Bruno Clarkson4

Rhinella granulosa (Spix, 1824) is a bufonid species, orders, only Diptera has more aquatic taxa described which produces highly toxic skin secretions (Jared and (Short, 2017). The two largest water beetle families in Antoniazzi, 2009) through dermal granular parotoid biodiversity, Dytiscidae and Hydrophilidae, have more glands (Felsemburgh et al., 2009), affording protection species than either Ephemeroptera or Plecoptera (Short, from predators as a primary defence mechanism 2017). (Clarke, 1997). Despite the large number of reports Hydrophilidae sensu Hansen (1999) currently regarding as prey and predators (Cortez- comprises ca. of 2840 living species in 169 genera Gómez et al., 2015), posing as key elements of both worldwide distributed (Short and Fikáček, 2011). terrestrial and aquatic food chains, composing diets of This family is commonly known as “water scavenger , and even carnivorous plants beetle” because of the feeding habits. Adult usually (Toledo et al., 2007), necrophagy, i.e, consumption of feed on decaying organic matter, but also may prey on dead , has frequently been underestimated or , small fishes or tadpoles (Balfour-Browne, 1910; minimized (DeVault and Krochmal, 2002), with very Balduf, 1935). Larvae are usually predacious and feed few known reports from Brazilian biomes. on other invertebrates such as crustaceans, larvae Aquatic form a complex ecological guild and adults, annelids and snails; and vertebrates such as comprising representatives of at least 30 Coleoptera small fishes and tadpoles (Hansen, 1991). Cannibalism families, consequence of several macroecological shifts has been recorded in many species (Balduf, 1935; from terrestrial habitats throughout more than 300 Ma Archangelsky, 1997). Tropisternus Solier, 1882 is a of evolutionary history (Short, 2017; Toussaint et al., common genus of Hydrophilidae in the New World, 2017). There are more than 13000 described species living in lentic freshwater habitats, such as ponds, pools, of Coleoptera considered aquatic and, among insect marshes, dams, wetlands and lake shores. Usually they are found associated with the aquatic vegetation, leaf- litter and/or several kinds of water bodies on bottom substrate (Hansen, 1991). The genus currently comprises 63 described species occurring from Argentina to Canada 1 Marcos Daniel Institute, Rua Fortunato Ramos 123, CEP (Hansen, 1991, 1999; Short and Fikáček, 2013). 29.055-290, Vitória, ES, Brazil. The Dytiscidae family has 4440 species (Nilsson 2 Universidade do Federal do Rio de Janeiro, Museu Nacional, Departamento de Invertebrados, Laboratório de Carcinologia, and Hájek, 2018) in 188 genres with a cosmopolitan Quinta da Boa Vista S/N, CEP 20940-040, Rio de Janeiro, distribution (Miller and Bergstein, 2016). This family RJ, Brazil. is commonly known as “diving beetle” because of the 3 Universidade Federal do Rio de Janeiro, Instituto de Biologia, air storage under the elytra similar to the divers oxygen Departamento de Zoologia, Laboratório de Entomologia, tanks (Miller and Bergstein, 2016), also is common to P.O. Box 68044, CEP 21941–971, Rio de Janeiro, RJ, Brazil. add carnivores or predaceous in front of the name due 4 Universidade Federal do Paraná, Setor de Ciências Biológicas, to their feeding habits. The larvae are ravenous fluid- Departamento de Zoologia. Laboratório de Sistemática e Bioecologia de Coleoptera, P.O. Box 19020, CEP 81531-980, feeding predators feeding on a wide range of prey Curitiba, PR, Brazil. including small vertebrates and in case of food shortage * Corresponding author. E-mail: [email protected] can resort to cannibalism (Miller and Bergstein, 2016; 870 Thiago Silva-Soares et al.

Lauren et al., 2014). Adults are carnivorous feeding on captured prey or recently dead material (Miller and Bergstein, 2016). succinctus (Aubé, 1838) is a common species in New World (Braga, 2014) living in lentic freshwater habitats, such as ponds, pools, marshes, dams, wetlands and lakeshores. Usually they are associated with a leaf-litter substrate. There is no information on feeding to this species, the closest would be the work of Velasco and Millan (1998) on the feeding of the Nearctic species (Gray, 1831), which indicated an exclusive scavenger habit with preference of soft organisms with thin cuticle, such as immature larvae of some mayflies, beetles, dragonflies, tadpoles or fishes in detriment of common in the rest of family. There are some records on vertebrates scavenging anurans, with several reports for mammals, birds, reptiles and other amphibians as predators (see compilation in Toledo et al., 2007; Oliveira et al., 2017). However, regarding amphibians as dead preys for scavenger invertebrates, reports decrease in numbers. Crustaceans are amongst the main known to consume vertebrates, amphibians included (McCormick and Polis, 1982; Wells, 2007). For instance, crabs as (e.g.) Trichodactylus fluviatilis Latreille, 1828 have been reported scavenging adult anurans, including the bufonid (Mageski et al., 2013, Segadilha Figure 1. A. Necrophagy by Tropisternus (Pristoternus) and Silva-Soares, 2015), as well as anuran egg clutches apicipalpis (family Hydrophilidae) and Thermonectus succinctus (family Dytiscidae) in carcass of Rhinella (Nogueira-Costa et al., 2016). Another crustacean granulosa; B. Detail of T. (Pristoternus) apicipalpis eating the scavenger is the crayfish Procambarus clarkii (Girard, skin of R. granulosa. Photos by Thiago Silva-Soares. 1852) reported by Banci et al., (2013) feeding upon a dead bufonid, Rhinella mirandaribeiroi (Gallardo, 1965). Furthermore, water as Lethocerus spp. and Megadytes (Bofurcitus) lherminieri (Guérin- WGS84), at 783 m above sea level, in the municipality Méneville, 1829) have also been reported as anuran of Cafarnaum, state of Bahia, north-eastern Brazil. scavengers (Figueira-de-Andrade et al., 2010; Zina et The bufonid and beetles were collected and preserved al., 2012; Rocha et al., 2014; Tortorelli et al., 2016). in 70% alcohol solution. The was deposited We herein report the first record of necrophagy for under the voucher (MBML 8897) in the Tropisternus (Pristoternus) apicipalpis (Chevrolat, Collection of the Instituto Nacional da Mata Atlântica, 1834), family Hydrophilidae, and Thermonectus municipality of Santa Teresa, Espírito Santo State, succinctus (Aubé, 1838), family Dytiscidae, on Rhinella Brazil. Material examined information: Bufonidae: 1 granulosa (Spix, 1824). The beetles were eating the male spec. [alcohol 70% solution]: “Rhinella granulosa/ carcass (Figs. 1A, B), which were in an initial stage of (Spix, 1824)/ T Silva-Soares det. 2016/ MBML 8897”. decaying (fresh stage, according to Braig and Perotti, The beetles were deposited in the Entomological 2009). Moreover, it is worth of note that one unidentified Collection Pe. J.S. Moure, Universidade Federal do and not collected was also scavenging the dead R. Paraná (UFPR), Curitiba, Paraná State, Brazil (DZUP). granulosa (Fig. 1B). Observations of this behaviour and Material examined information: DZUP Coleoptera: (3 photographic records were taken at about 6:50 p.m. on spec.) “BRAZIL: Bahia, Cafarnaum,/ 11°40.857’ S, 3 March 2016, on a temporary pond situated laterally 41°24.039’ W/ 03.III.2016, 783 m a.s.l./ T Silva-Soares a dust road (238293.34 E, 8707615.38 S, Datum and JL Segadilha col.”. Hydrophilidae: 1 male spec. Necrophagy on Rhinella granulosa by aquatic beetle species, Northeastern Brazil 871

[pinned and dissected]: “Tropisternus (Pristoternus) Devault, T.L., Krochmal, A.R. (2002): Scavenging by snakes: an apicipalpis/ (Chevrolat, 1834)/ B Clarkson det. 2017// examination of the literature. Herpetologica 58(4): 429–436. DZUP 469250”; Dytiscidae: 2 males spec. [pinned]: Felsemburgh, F.A., Almeida, P.G., Carvalho-e-Silva, S.P., de Brito-Gitirana, L. (2009): Microscopical methods promote the “Thermonectus succinctus/ (Aubé, 1838)/ RB Braga understanding of the integument biology of Rhinella ornata. det. 2017// DZUP 469251” and “DZUP 469252”. Micron 40(2): 198–205. These data in behavioural biology is herein presented Figueira-de-Andrade, C.A., Santana, D.J., de Carvalho-e-Silva, with precise identification of both beetles and toad. The S.P. (2010): Predation on Scinax x-signatus (Anura: Hylidae) identification was done by specialists in the of by the giant water bug Lethocerus annulipes (: each of the species involved in this study. 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Accepted by Javier Cortés Suárez