Herpetology Notes, volume 14: 581-584 (2021) (published online on 29 March 2021)
Deadly food: Physical injury in Scinax nasicus (Cope, 1862) (Anura: Hylidae) caused by a dung beetle (Coleoptera: Scarabaeidae)
Rafaela Thaler1,*, Gabriel S. Gonçalves1, Fernando Paiva1 and Vanda L. Ferreira1
Anurans play an important role in many food webs possible predation (Toledo, 2005; Wizen and Gasith, as they are both consumers and prey (Toledo et al., 2011a, b) 2005; Pombal et al., 2007). Organisms must assess risks Around 19:00 h on 13 March 2019, we encountered during foraging to survive (Mukherjee and Heithaus, an adult S. nasicus on the ground with a conspicuous 2013); indeed, prey may pose a danger to predators volume in the dorsal region of the body, during due to their body size or shape, defensive behaviours, nocturnal fieldwork at Nhumirim Ranch (18.9880°S, chemical defences, dangerous body structures, skin 56.6190°W; datum WGS84) in the Pantanal subregion toxins, and/or inexperience of the predator (Phillips et of Nhecolândia, a municipality in Corumbá, Mato al., 2003; Toledo et al., 2011; Sugiura and Sato, 2018). Grosso do Sul, Brazil. This ranch is seasonally flooded, Predators may therefore be injured or even killed by with water level and hydroperiod depending on local their prey, especially when they ingest prey larger rainfall and the height of the Paraguay River. The ranch than their own bodies (Mukherjee and Heithaus, 2013; contains about 100 lakes covering 4310 ha from January Nogueira et al., 2013). Little is known, however, about to April during wet years but may dry completely in anuran behaviours for reducing risks or even injuries some years (Hamilton et al., 1996; Mourão et al., 1998, when consuming dangerous prey (e.g., Waterhouse, 2013). The landscape of the ranch is composed of a 1974; Greenlees et al., 2010; Sugiura and Sato, 2018). mosaic of vegetated areas during the dry season (April Scinax nasicus (Cope, 1862), the Lesser Snouted to September), including forest, cerrado (savannah), Treefrog, is a small nocturnal hylid native to Argentina, cerradão (dense savannah), floodable grassland, and Bolivia, Brazil, Paraguay, and Uruguay (Frost, 2020). ponds (Alho et al., 1987; Barros, 2001). This species is found mainly in arboreal habitats, using We identified the frog by its external morphology, bromeliad leaf axils, herbaceous vegetation, shrubs, such as the acuminated snout, short hindlimbs with and even human habitations as their microhabitats tibiotarsal articulation reaching the eye, poorly (Ávila and Ferreira, 2004). Their diet is composed developed metatarsal tubercles, brownish to yellowish- predominantly of insects belonging to the orders Diptera, green dorsum with longitudinal bands and dark blotches, Hymenoptera, and Coleoptera (Duré, 1999; Cossovich and yellowish dorsolateral region with dark bands et al., 2011), which are food resources commonly (Uetanabaro et al., 2008; Ziegler and Maneyro, 2008). consumed by anurans (Mollov and Delev, 2020). The The anuran was relatively immobile when captured order Coleoptera is the largest and richest group of and had limited muscle reactions when handled. We insects, having a wide geographical distribution and euthanised the individual in the laboratory by injecting using several microhabitats (Rafael et al., 2012). These thiopental sodium to examine this unusual finding. factors allow coleopterans to co-occur with frogs, which We studied the anuran (snout–vent length, 31.57 facilitates encounters in different stages of life and mm; body mass, 1.747 g) in more detail by performing a gross autopsy and found a dung beetle in the subcutaneous layer. We verified a continuous lesion in 1 Instituto de Biociências, Universidade Federal de Mato Grosso the dorsolateral part of the body behind the left eye. A do Sul, Campo Grande, Mato Grosso do Sul 79070-900, cut in the skin about 9 mm long exposed a protruding Brazil. antennae and rostral region of a dead insect (Fig. 1A). * Corresponding author. E-mail: [email protected] A subsequent necropsy found that the insect, a beetle, © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. pierced the stomach wall, peritoneum, and the external 582 Rafaela Thaler ����l. oblique muscle after being swallowed by the amphibian Grosso do Sul Federal University (ZUFMS) under and moved into a supine position through the dorsal voucher numbers ZUFMS-AMP12504 and ZUFMS- subcutaneous lymphatic sac until tearing the skin and COL00205, respectively. lodging itself in the dorsal region of the amphibian We believe that this event is attributed to frogs (Fig. 1B–E). The beetle belonged to the subfamily swallowing their prey whole and often still alive Aphodiinae (body length and mass, 12.93 mm and 0.148 (Waterhouse, 1974; Monroy and Nishikawa, 2011). g, respectively). The frog was fixed in 10% formalin, The beetle likely injured its predator with its tough and the frog and beetle were preserved in 70% alcohol exoskeleton and strongly sclerotised pointed jaws and and deposited in the Zoological Collection of the Mato legs in an attempt to escape (Rafael et al., 2012). The
Figure 1. (A) Adult Scinax nasicus displays a deformation in the dorsal region of the body due to the presence of a dung beetle (subfamily Aphodiinae). Perforations caused by the beetle (B) behind the left eye and in the (C) external oblique muscle and (D) stomach wall. (E) Removal of the beetle from the subcutaneous region and the perforation in the external oblique muscle (white arrow). The scale bar applies only to panel (A). Photographs by F. Paiva. Deadly food: Physical injury in Scinax nasicus caused by a dung beetle 583 large size of the beetle relative to the predator may ours therefore provide data with implications for the have contributed to its attempt to escape. The frog was future understanding of interactions between frogs and still alive when captured, but an injured individual can potentially dangerous prey. become more vulnerable to competitors or predators (Mukherjee and Heithaus, 2013). The severe physical Acknowledgements. We thank Andressa Figueiredo de Oliveira injuries to the stomach wall, peritoneum, abdominal for identifying the beetle, Noeli Zanella for the suggestions muscles, and skin would have probably been fatal to the in the pre-peer review, and two anonymous reviewers for the recommendations. We appreciate the logistical support frog. of Embrapa-Pantanal. Thanks are also due to the Instituto We found two similar records of ruptured stomach Chico Mendes de Conservação da Biodiversidade/Sistema de walls: one of a dead Australian frog with ruptured Autorização e Informação em Biodiversidade (ICMBio/SISBIO), stomach and body walls after the ingestion of a scarab for the collection and transport permits for the specimens beetle (Waterhouse, 1974), and the other of dead Round- (#63916-1), and the Animal Use Ethics Committee (CEUA/ tailed Horned Lizards with stomach walls ruptured UFMS #941/2018). We also thank the Conselho Nacional de by black scarabs (Sherbrooke, 2002). We also found Desenvolvimento Científico e Tecnológico (CNPq) for project records of toads that vomited bombardier beetles due to financial support (CNPq #409003/2018-2), RT’s master’s fellowship (#133289/2019-2), GSG’s scholarship (PIBIC their chemical defences (Dean, 1980; Sugiura and Sato, #139922/2019-9), and VLF’s (PQ2/CNPq #309305/2018-7), and 2018) and of a young captive Nile crocodile that died FP’s (PQ2/CNPQ #306728/2016-8) researcher fellowships. This of poisoning after ingesting darkling beetles (Perelman study was financed in part by the Fundação Universidade Federal and Chikatunov, 2010). This low number of records of de Mato Grosso do Sul – UFMS/MEC – Brazil, Coordenação de scarab beetles harming their predators may be due to the Aperfeiçoamento de Pessoal de Nível Superior (CAPES) – Brazil difficulty of observing such ephemeral events in nature. (Finance #001) and Fundação de Apoio ao Desenvolvimento do Previous records are predominantly for captive animals. Ensino, Ciência e Tecnologia do Estado de Mato Grosso do Sul The scarcity of reports suggests that these events are (FUNDECT) (#084201 and #084/2015). infrequent. Coleoptera are part of the diet of many organisms (Young, 2015) and are frequently consumed References by anurans (Ceron et al., 2019). Alho, C.J.R., Campos, Z.M.S., Gonçalves, H.C. (1987): Ecologia Reports of Scarabaeidae consumption are less frequent de capivara (Hydrochaeris hydrochaeris, Rodentia) do Pantanal. for Hylidae than Bufonidae species (e.g., Antoniazzi et I – Habitats, densidades e tamanho de grupo. Revista Brasielira al., 2013; Young, 2015). Food items in dietary studies of de Biologia 47: 87–97. anurans, however, have rarely been identified to family Antoniazzi, C.E., López, J.A., Duré, M., Falico, D.A. (2013): Alimentación de dos especies de anfibios (Anura: Hylidae) en la or species levels (Young, 2015) but instead to order level estación de bajas temperaturas y su relación con la acumulación due to the degree of digestion (e.g., Duré 1999; Kittel de energía en Santa Fe, Argentina. Revista de Biología Tropical and Solé, 2015; Blanco-Torres et al., 2017; Michelin 61(2): 875–886. et al., 2020). Future assessments should therefore Ávila, R.W., Ferreira, V.L. (2004): Riqueza e densidade de investigate if hylids avoid feeding on scarabs more vocalizações de anuros (Amphibia) em uma área urbana de than do other anuran families or whether the number of Corumbá, Mato Grosso do Sul, Brasil. Revista Brasileira de studies comprising taxonomic levels lower than order Zoologia 21(4): 887–892. are disproportionate amongst families. Barros, A.T.M. (2001): Seasonality and relative abundance of Tabanidae (Diptera) captured on horses in the Pantanal, Brazil. In summary, our record provides the first evidence Memórias do Instituto Oswaldo Cruz 96(7): 917–923. of physical injury to S. nasicus caused by a beetle of Blanco-Torres, A., Duré-Pitteri, M.I., Bonilla, M.A. (2017): the family Scarabaeidae. We attribute this uncommon Trophic ecology of Scinax rostratus (Peters, 1863) and Scinax find to the morphological defences of the beetle, such ruber (Laurenti, 1768) (Anura: Hylidae) in tropical dry forests as rigid and pointed body structures and the large body of northern Colombia. Herpetology Notes 10: 405–409. relative to the frog. Events like the one described here Ceron, K., Oliveira-Santos, L.G.R., Souza, C.S., Mesquita, D.O., are rarely reported, even though anurans frequently Caldas, F.L., Araujo, A.C., Santana, D.J. (2019): Global patterns consume Coleoptera, which may be due to the difficulty in anuran–prey networks: structure mediated by latitude. Oikos 128(11): 1537–1548. of finding such ephemeral events and to their infrequent Cossovich, S., Aun, L., Martori, R. (2011): Análisis trófico de la occurrence. We also suggest investigating the possibility herpetofauna de la localidad de Alto Alegre (Depto. Unión, of Scarabaeidae consumption amongst anuran families, Córdoba, Argentina). Cuadernos de Herpetología 25: 11–19. which could provide insight into the risks to anurans Dean, J. (1980): Encounters between bombardier beetles and two during foraging activity. Specific descriptions such as species of toads (Bufo americanus, B. marinus. Speed of prey- 584 Rafaela Thaler ����l.
capture does not determine success. Journal of Comparative Perelman, B., Chikatunov, V. (2010): Intoxication of young Physiology 135: 41–50. Crocodiles in captivity due to the ingestion of darkling beetles Duré, M.I. (1999): Interrelaciones en los nichos tróficos de dos Blaps nitens laportei Ardoin (Coleoptera: Tenebrionidae). Israel especies sintópicas de la familia Hylidae (Anura) en un área Journal of Veterinary Medicine 65(3): 100–102. subtropical de Argentina. Cuadernos de Herpetología 13(1/2): Phillips, B.L., Brown, G.P., Shine, R. (2003): Assessing the potential 11–18. impact of cane toads on australian snakes. Conservation Biology Frost, D.R. (2020): Amphibian Species of the World: an Online 17(6): 1738–1747. Reference. Version 6.0. American Museum of Natural History, Pombal Jr, J.P. (2007): Notas sobre predação em uma taxocenose New York, USA.
Accepted by Aldemar Acevedo