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Native Anuran Species As Prey of Invasive American Bullfrog, Lithobates Catesbeianus, in Brazil: a Review with New Predation Records 1,2,*Fabrício H

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Native Anuran Species As Prey of Invasive American Bullfrog, Lithobates Catesbeianus, in Brazil: a Review with New Predation Records 1,2,*Fabrício H Offcial journal website: Amphibian & Reptile Conservation amphibian-reptile-conservation.org 13(2) [General Section]: 217–226 (e207). Native anuran species as prey of invasive American Bullfrog, Lithobates catesbeianus, in Brazil: a review with new predation records 1,2,*Fabrício H. Oda, 3Vinicius Guerra, 4Eduardo Grou, 5Lucas D. de Lima, 5Helen C. Proença, 6Priscilla G. Gambale, 4,5Ricardo M. Takemoto, 7Cauê P. Teixeira, 7Karla M. Campião, and 8Jean Carlo G. Ortega 1Departamento de Química Biológica, Programa de Pós-graduação em Bioprospecção Molecular, Universidade Regional do Cariri, Campus Pimenta, 63105-000, Crato, Ceará, BRAZIL 2Departamento de Química Biológica, Laboratório de Zoologia, Universidade Regional do Cariri, Campus Pimenta, Crato, Ceará, BRAZIL 3Departamento de Ecologia, Laboratório de Herpetologia e Comportamento Animal, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus Samambaia, Goiânia, Goiás, BRAZIL 4Centro de Ciências Biológicas, Núcleo de Pesquisas em Limnologia, Ictiologia e Aquicultura, Laboratório de Ictioparasitologia, Universidade Estadual de Maringá, Maringá, Paraná, BRAZIL 5Centro de Ciências Biológicas, Programa de Pós-graduação em Biologia Comparada, Universidade Estadual de Maringá, Paraná, BRAZIL 6Universidade Estadual de Mato Grosso do Sul, Dourados, Mato Grosso do Sul, BRAZIL 7Departamento de Zoologia, Laboratório de Ecologia de Interações Antagonistas, Universidade Federal do Paraná, Centro Politécnico, Curitiba, Paraná, BRAZIL 8Departamento de Ecologia, Programa de Pós-graduação em Ecologia e Evolução, Instituto de Ciências Biológicas, Universidade Federal de Goiás, Campus Samambaia, Goiânia, Goiás, BRAZIL Abstract.—The American Bullfrog (Lithobates catesbeianus) is widely distributed throughout the world as an invasive species, and causes negative impacts on the fauna resulting from its voracious predatory activity. This study documents two new predation reports and reviews the previous predation reports of the American Bullfrog on native Brazilian anurans. Twenty-one species of native anurans were recorded as American Bullfrog prey in Brazil. A positive correlation was found between the number of native anurans preyed on by American Bullfrog and the respective family or number of species per genus. Most of the prey species are small or medium-sized, and the results suggest that the generalist diet and intraguild predation may have favored the widespread establishment of the American Bullfrog. Keywords. Amphibia, Atlantic Forest, biological invasion, conservation, global change, intraguild predation, exotic species Citation: Oda FH, Guerra V, Grou E, de Lima LD, Proença HC, Gambale PG, Takemoto RM, Teixeira CP, Campião KM, Ortega JCG. 2019. Native anuran species as prey of invasive American Bullfrog, Lithobates catesbeianus, in Brazil: a review with new predation records. Amphibian & Reptile Conservation 13(2) [General Section]: 217–226 (e207). Copyright: © 2019 Oda et al. This is an open access article distributed under the terms of the Creative Commons Attribution License [Attribution 4.0 International (CC BY 4.0): https://creativecommons.org/licenses/by/4.0/], which permits unrestricted use, distribution, and reproduction in any me- dium, provided the original author and source are credited. The offcial and authorized publication credit sources, which will be duly enforced, are as follows: offcial journal title Amphibian & Reptile Conservation; offcial journal website: amphibian-reptile-conservation.org. Received: 8 February 2017; Accepted: 23 June 2019; Published: 20 December 2019 Introduction environments has direct (e.g., predation and competition) and indirect (e.g., parasites, disease introduction, and Biological invasions represent a major threat to natural biotic homogenization) impacts on biodiversity (Batista ecosystems and their respective biodiversity, human 2002; Batista et al. 2015; Kiesecker and Blaustein 1998; health, and food security (IUCN 2012). In this context, Kraus 2009). the American Bullfrog, Lithobates catesbeianus (Shaw, Lithobates catesbeianus is a voracious predator whose 1802), is a globally widespread introduced species (Lowe diet includes a wide variety of prey (Boelter and Cechin et al. 2004). It is native in North America, occurring 2007; Boelter et al. 2012; Silva et al. 2009). Juveniles from eastern Canada and the central and eastern United feed mainly on insects (Silva et al. 2009), whereas adults States to northeastern Mexico (Quiroga et al. 2015). prey upon invertebrates and small vertebrates, such as The introduction of L. catesbeianus in non-native fsh, reptiles, birds, and mammals (Quiroga et al. 2015). Correspondence. *[email protected] (FHO), [email protected] (VG), [email protected] (EG), lucasdu- [email protected] (LDL), [email protected] (HCP), [email protected] (PGG), [email protected] (RMT), [email protected] (CPT), [email protected] (KMC), [email protected] (JCGO) Amphib. Reptile Conserv. 217 December 2019 | Volume 13 | Number 2 | e207 Impact of bullfrogs on native anurans in Brazil American Bullfrogs are considered opportunistic feeders, invasive American Bullfrog Lithobates catesbeianus in also preying on amphibians, including conspecifcs and Brazil. The sources included articles or natural history other species (Silva et al. 2011; Toledo et al. 2007). notes published in Herpetological Review (1967–2018), The American Bullfrog is now established in Herpetological Bulletin (2008–2018), Herpetology nearly 40 countries around the world (Frost 2019; Notes (2008–2018), and South American Journal of Kraus 2009). In Brazil, the frst specimens were Herpetology (2006–2018). Searches were also conducted introduced in 1935 for commercial exploitation at in Web of Science using the following query: (“Rana the municipality of Itaguaí, Rio de Janeiro state catesbeiana” OR “Lithobates catesbeianus”) AND (Vizotto 1984). The introduction of the American (“diet” OR “feeding biology” OR “predation”), applied in Bullfrog for commercial frog farming was due to its the feld “topic” on 30 December 2018, without applying fast reproduction and greater development in captivity any flters for year or other parameters. Considering compared to native species. It occurs mainly in the that predation attempts would not necessarily result in a southern and southeastern Brazilian states because of predation event (Toledo et al. 2007), reports of predation its easy adaptation to the climatic conditions (Vizotto attempts in the feld, laboratory experiments, or captivity 1984). Approximately 2,000 commercial frog farms were not included. Masters and doctoral papers in digital were active in the early 1990s in Brazil, but many format were obtained from the library databases of closed their activities because of low proftability Brazilian universities (especially Universidade Estadual (Lima and Agostinho 1988), which led to American Paulista and Universidade Regional de Blumenau) by Bullfrog specimens being abandoned or released into using the search terms mentioned above in the Google the natural environments, and consequently several search engine. accidental invasions have occured in Brazil (Both et The Web of Science query resulted in 159 studies, al. 2011). three of which met the criteria and were included in the Populations of Lithobates catesbeianus are now study. Eight additional predation records were selected for known to be present in 155 Brazilian municipalities inclusion in the study by searching the selected journals (Both et al. 2011; Instituto Horus 2016), a context in (six studies) and the library databases of Brazilian which many studies have revealed the localized impacts universities (two studies). Information was extracted of its predatory activity on native anuran fauna (Batista from each diet analysis (i.e., the diet was described et al. 2015; Boelter and Cechin 2007; Boelter et al. through the analyses of stomach contents or predation 2012; Leivas et al. 2012; Silva et al. 2011). In addition, records), study location, anuran prey species, geographic global-scale studies have demonstrated trophic niche- range, and body size. The geographic range follows the width shifts in bullfrog populations from both native and list of anuran species for each Brazilian federal state invaded areas (Bissattini and Vignoli 2017), as well as the and the biomes proposed in Toledo and Batista (2012). effects of the interactions between bullfrogs and crayfsh The body sizes of anuran species follow the size values on native amphibians (Bissattini et al. 2018, 2019; Liu available in Uetanabaro et al. (2008) and Haddad et et al. 2018). However, studies summarizing data on the al. (2013). The spatial distribution map of Lithobates predation of native anurans by American Bullfrogs have catesbeianus invasive populations and predation reports yet to be presented; therefore, knowledge on the impact were generated with 155 occurrence points for American and the native anuran species preyed upon by such an Bullfrog in Brazil, obtained from Both et al. (2011) and invasive frog may beneft our understanding of their Instituto Horus (2016). predator-prey relationships. Herein, the predation of Boana raniceps and Data Analysis Phyllomedusa distincta by males of Lithobates catesbeianus are reported, and the available literature The relation between the number of native anuran on the predation of native anurans by the invasive frog species preyed upon by the American Bullfrog and the L. catesbeianus
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