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Revista latinoamericana de herpetología

versión On-line ISSN 2594-2158

Rev. latinoam. herpetol. vol.5 no.4 Ciudad de México oct./dic. 2022  Epub 26-Jun-2023

https://doi.org/10.22201/fc.25942158e.2022.4.551 

Scientific notes

New Predation Records on Thoropa miliaris (Anura: Cycloramphidae), with a Review of Known Predators

Nuevos registros de depredación de Thoropa miliaris (Anura: Cycloramphidae), con una revisión de los depredadores conocidos

Henrique J. Oliveira1  * 

Carlos H. O. Nogueira2 

Paulo S. Amorim1 

André C. Guaraldo1  3 

Henrique C. Costa1 

1Universidade Federal de Juiz de Fora, Programa de Pós-Graduação em Biodiversidade e Conservação da Natureza. 36036-900, Juiz de Fora, MG, Brazil.

2Universidade Federal de Mato Grosso do Sul, Programa de Pós-Graduação em Biologia Animal. 79070-900, Campo Grande, MS, Brazil.

3Universidade Federal do Paraná, Departamento de Zoologia. 81531-980, Curitiba, PR, Brazil.


Abstract

The rock river frog Thoropa miliaris (Cycloramphidae) is a saxicolous species endemic to the Atlantic Forest. There is scarce literature on potential predators of this species, which is likely related to the difficulty of recording its predatory interactions. In this paper, we report opportunistic records of predation on T. miliaris by the snake Chironius laevicollis (Colubridae), spiders of the genus Ctenus (Ctenidae), and the bird Furnarius rufus (Furnariidae). In addition, we compiled the reports of predation on T. miliaris from current published data.

Key words: Atlantic Forest; diet; Eltonian shortfall; trophic ecology

Resumen

La rana de las piedras Thoropa miliaris (Cycloramphidae) es una especie saxícola endémica del Bosque Atlántico. La información sobre los posibles depredadores de esta especie es escasa en la literatura, un hecho posiblemente relacionado con la dificultad de registrar eventos de interacción entre predadores y presas. En este trabajo registramos diversos eventos predatorios oportunistas sobre T. miliaris por la serpiente Chironius laevicollis (Colubridae), por arañas del género Ctenus (Ctenidae) y por el ave Furnarius rufus (Furnariidae). Además, recopilamos los registros de depredación de las especies publicados hasta ahora.

Palabras claves: déficit eltoniano; dieta; ecología trófica; Bosque Atlántico

Data on predation are important to reduce the Eltonian shortfall― the lack of knowledge on biotic interactions (Hortal et al., 2015) ―, but in nature, such data are recorded only occasionally (Menegucci et al., 2020). Anurans are an important part of the food web, as the prey of many vertebrate and invertebrate species (Toledo et al., 2007; Hocking & Babbitt, 2014). Brazil is the country with the greatest anuran diversity (Segalla et al., 2021; Frost, 2022), but the knowledge of biotic interactions of Brazilian anurans is deficient, even for common species like Thoropa miliaris (Spix, 1824), an endemic species to rocky environments in the Brazilian Atlantic Forest (Giaretta & Facure, 2004; Feio et al., 2006). In this work, we report opportunistic records of predation on T. miliaris by a snake, spiders, and a bird. We also compile the literature data on predators recorded for this species.

On 18 August 2014, at 20:04, CHON found a dead male snake Chironius laevicollis (Wied, 1824) (Colubridae) of 2.10 m snoutvent length at the Tombo D’água waterfall (Fig. 1A) (district of Mocotó do Imbé, municipality of Campo dos Goytacazes, state of Rio de Janeiro, Brazil; 21.81367° S, 41.75552° W, WGS84, 282 m a.s.l.). Dissection of the snake’s abdomen revealed a partially digested T. miliaris (Fig. 1B). Predator and prey were not collected due to the degree of decomposition, but we were able to identify both species based on their overall morphology and color pattern (Dixon et al., 1993; Feio et al., 2006).

Photos by PSA.

Figure 1 A) Specimen of Chironius laevicollis (Colubridae) found dead in Campos dos Goytacazes, Rio de Janeiro, Brazil. B) Thoropa miliaris (Cycloramphidae) removed from the stomach of C. laevicollis. Photos by CHON. C) Thoropa miliaris being preyed upon by a Ctenus sp. (Ctenidae) spider in Campos dos Goytacazes, Rio de Janeiro, Brazil. D) Thoropa miliaris being preyed on by a Ctenus cf. medius (Ctenidae) in Campos dos Goytacazes, Rio de Janeiro, Brazil. Photos by CHON. E) and F) Furnarius rufus (Furnariidae) preying on T. miliaris in Juiz de Fora, Minas Gerais, Brazil. 

Fotos de PSA.

Figura 1 A) Individuo de Chironius laevicollis (Colubridae) encontrado muerto en el município de Campos dos Goytacazes, estado de Rio de Janeiro, Brasil. B) Individuo de Thoropa miliaris (Cycloramphidae) encontrado en el estómago de C. laevicollis, Campos dos Goytacazes, Rio de Janeiro, Brasil. Fotos de CHON. C) Individuo de T. miliaris siendo presa de una araña del género Ctenus sp. (Ctenidae) en Campos dos Goytacazes, Rio de Janeiro, Brasil. D) Individuo de T. miliaris siendo presa de una araña del género Ctenus cf. medius (Ctenidae) en Campos dos Goytacazes, Rio de Janeiro, Brasil. Fotos de CHON. E) y F) Individuo de Furnarius rufus (Furnariidae) predando un individuo de T. miliaris en el município de Juiz de Fora, estado de Minas Gerais, Brasil. 

At this same locality, CHON recorded two additional predation events on T. miliaris by spiders of the family Ctenidae: Ctenus sp. and Ctenus cf. medius Keyserling, 1891, identified by the spider taxonomist Leonardo Carvalho, Universidade Federal do Piauí, Brazil. The first record was on 19 February 2020, at 18:35 (21.82724° S, 41.74726° W; WGS84; 174 m a.s.l.; Fig. 1C), and the second on 16 June 2021, at 19:46 (21.81449° S, 41.75748° W; Fig. 1D). The T. miliaris individuals were collected and deposited in the Coleção Herpetológica do Norte Fluminense (CHNF 0897 and CHNF 0975, respectively).

On 21 February 2020, at 12:10, PSPA recorded a T. miliaris being preyed by a juvenile Rufous hornero, Furnarius rufus (Gmelin, 1788) (Furnariidae) in an urban environment near the hospital of the Universidade Federal de Juiz de Fora, municipality of Juiz de Fora, state of Minas Gerais, Brazil (21.78553° S, 43.36787° W, WGS84, 878 m a.s.l.; Fig. 1E). The T. miliaris was initially observed beside a paved road with little traffic, when the bird appeared and repeatedly pecked the frog on its dorsum, venter, and head. The frog attempted to escape several times, but the bird held it with its beak. The bird immobilized the frog and swallowed it alive (Fig. 1F). The bird was subsequently observed for approximately 40 minutes from a distance of 30 cm, but no regurgitation was recorded (see record video at https://doi. org/10.5281/zenodo.6954386). Prey identity was confirmed by Diego J. Santana (Universidade Federal do Mato Grosso do Sul, Brazil).

We reviewed literature records of predators of T. miliaris in Google Scholar on 28 April 2022, searching for the expression “predation OR predator OR prey AND ‘Thoropa miliaris’” in English, Spanish (depredación OR presa OR depredador), and Portuguese (predação OR presa OR predador), and found 267 results. Of these, only eight showed T. miliaris as the prey. We also searched issues of Herpetological Review from 1967-2022, finding four additional records. In addition, we searched the authors' pdf libraries. All reports are shown in Table 1.

Table 1 List of predators of Thoropa miliaris (Anura: Cycloramphidae) based on the authors’ data and literature review. 

Tabla 1 Lista de depredadores de Thoropa miliaris (Anura: Cycloramphidae) basada en los datos propios de los autores y en una revisión de la literatura. 

Predator identification Life stage of prey Environment Source
Arachnida
Cteniza sp. Latreille, 1829 Post-metamorphic Forest Pertel et al., 2010
Ctenus cf. medius Keyserling, 1891 Post-metamorphic Forest This study
Ctenus sp. Post-metamorphic Forest This study
Trechalea sp. Tadpole Forest Diniz et al., 2020
Anura
Cycloramphus boraceiensis (Heyer, 1983) Tadpole Forest Hartmann et al., 2003
Thoropa miliaris (Spix, 1824) (Tadpole) Egg Forest Giaretta & Facure, 2004
Aves
Furnarius rufus (Gmelin, 1788) Post-metamorphic Urban This study
Insecta
Tropisternus sp. (Larvae) Tadpole Forest Siqueira et al., 2006
Squamata
Bothrops jararaca (Wied, 1824) Post-metamorphic Forest Sazima, 1992
Chironius bicarinatus (Wied, 1820) Post-metamorphic Forest Roberto & Souza, 2020
Chironius flavolineatus (Jan, 1863) Post-metamorphic Not informed Pinto et al., 2008; Roberto & Souza, 2020
Chironius fuscus (Linnaeus, 1758) Post-metamorphic Forest Marques & Sazima, 2004; Hartmann, 2005; Roberto & Souza, 2020
Chironius laevicollis (Wied, 1824) Post-metamorphic Forest This study
Erythrolamprus miliaris (Linnaeus, 1758) Post-metamorphic Forest Albolea, 1998; Marques & Sazima, 2004; Mônico et al., 2016; Burg, 2020
Erythrolamprus poecilogyrus (Wied, 1825) Post-metamorphic Not informed Pinto & Fernandes, 2004
Tropidurus torquatus (Wied, 1825) Unknown - Museum specimen Urban Mônico & Mônico, 2022

Snakes are among the most important predators of postmetamorphic anurans (Toledo et al., 2007). Most reports of predation on T. miliaris were by Chironius spp., a genus of frogeating species (Marques et al., 2016). Conversely, lizards are the least frequent vertebrate predators of frogs (Toledo et al., 2007). We found a single record of T. miliaris being preyed by a lizard (Mônico & Mônico, 2022): Tropidurus torquatus, a saxicolous species with a generalist diet (Gomides et al., 2013; Guimarães & Sbrek-Araujo, 2018). We also found two records of frogs preying on T. miliaris: i) tadpoles being preyed upon by Cycloramphus boraceiensis (Hartmann et al., 2003), and ii) egg cannibalism by conspecific tadpoles (Giaretta & Facure, 2004). Tadpoles were also preyed upon by larvae of the beetle Tropisternus sp., the only record of an insect preying on T. miliaris, despite Coleoptera being one of the most recorded invertebrate groups of anuran predators (Toledo, 2005). Arachnida is another frequently recorded invertebrate group of anuran predators (Toledo, 2005), although we found only two predation events, by a Cteniza sp. and Trechalea sp. (Pertel et al., 2010; Diniz et al., 2020).

Our records improve the information about the predation of post-metamorphic specimens of T. miliaris by the spider genus Ctenus, whose species often actively forage for anurans in leaf litter (Salvestrini & Gasnier, 2001; Menin et al., 2005). We also report the first avian predator of T. miliaris, the Rufous hornero, Furnarius rufus. Birds are common predators of postmetamorphic anurans (Toledo et al., 2007), but the absence of records for T. miliaris highlights the knowledge gaps on the biotic interactions of this relatively common, conspicuous, and abundant species.

Acknowledgments

The authors are grateful to Diego J. Santana (Universidade Federal de Mato Grosso do Sul) and Leonardo S. Carvalho (Universidade Federal do Piauí) for confirming species identification. To Juan Carrillo for the review of the Spanish text and Ross MacCulloch for the review of the English text. To the editor Katyuscia Araujo-Vieira and two anonymous reviewers for suggestions in a first version of this article. This study is partially funded by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) - Finance Code 001 (Master's scholarship to HJO and CHON, and PhD scholarship to PSA).

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Received: September 29, 2022; Accepted: November 09, 2022; Published: December 29, 2022

*Correspondence: henrique.bio22@gmail.com

Editor: Katyuscia Araujo-Vieira, Brasil.

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