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Home , Emperor Scorpion, Epictia borapeliotes, Furina, Liotyphlops albirostris, Mato Grosso blind snake, Pandinus

Herpetology Notes, volume 13: 49-55 (2020) (published online on 30 January 2020)

The blind Trilepida koppesi (Amaral, 1955) as prey of armadillo Euphractus sexcinctus (Linnaeus, 1758), with a review of predators

Silara Fatima Batista1,2,*, Kátia Gomes Facure3, and Otavio A. V. Marques1,2

Snakes are consumed by several predators, including Cláudio et al., 2017). Herein we present a new record vertebrates (e.g. Costa et al., 2009) and invertebrates of on this and summarize records of (e.g. Borges et al., 2016). Subterranean live predation on several other scolecophids (Table 1). underground for much of the time making it hard for In August 28, 2010, an individual of yellow armadillo predators to access them. Among all living snakes, (Euphractus sexcinctus (Linnaeus, 1758), body mass: the Scolecophidia are the most specialized to live 6.0kg), was collected during a field trip, ran over, on the underground (Greene, 1997). This group of snakes, access road (MGC 461, 19°11’57.2”S; 49°47’01.9”W) usually named blind snakes, is traditionally divided in to Gurinhatã, MG and destining the didactic collection , and (Greene, 1997; Vidal et al., 2010). The leptotyphlopid snakes are known as threadsnakes or wormsnakes due to their small and fine body (Adalsteinsson et al., 2009). In , it currently comprises three genera (Epictia, and Trilepida) and 18 species (Costa & Bérnils et al., 2018). The blind snake Trilepida koppesi (Amaral, 1955) occurs in the Brazilian Cerrado (Passos et al., 2006). The few data of natural history indicate that it begins its activity after the sunset mainly in the rainy period, and feeds primarily on ant larvae and pupae (Sawaya et al., 2008). There is only one predation data of this blind snake by Labyrinth frog (Vaz-e-Silva et al., 2003), but leptotyphlopids can be predated by several groups (McCormick and Polis, 1982; Greene, 1988;

1 Universidade Estadual Paulista “Júlio de Mesquita Filho”, Instituto de Biociências, Letras e Ciências Exatas, Departamento de Zoologia e Botânica, Rua Cristovão Colombo, 2265, Jardim Nazareth, CEP 15054-000 São José do Rio Preto, SP, Brazil. 2 Instituto Butantan, Laboratório de Ecologia e Evolução, Avenida Vital Brasil, 1.500, Butantã, CEP 05503-900 São Paulo, SP, Brazil. 3 Universidade Federal de Uberlândia, Instituto de Ciências Exatas e Naturais do Pontal, Rua 20, 1600, Tupã, CEP Figure 1. The specimen of Trilepida koppesi (total length = 38304-402 Ituiutaba, MG, Brazil. 362 mm) found in the stomach of Euphractus sexcinctus, in * Corresponding author: [email protected] dorsal (A) and ventral (B) view. 50 Silara Fatima Batista et al.

Kelehear, 2014 Kelehear, Pizzatto 2012 et al., 2003 Vaz-Silva et al., 1976 Hahn, et al.,O'Shea 2013 et al., 2010 Krysko

Rodriguez et al., 2018 Rodriguez2018 et al.,

Spawls et al., Spawls 2004 et al., 2013 Kusamba Barbo,2008 Rodriguez2018 et al., et al., 2012 Ray et al.,Arévalo-Paez 2015 Rodriguez-Robles and1993 Leal, Rodriguez2018 et al., Martinelli, 2009 Dryden, 1965

Arthropod Reference

(anurans) (anurans) (anurans) (anurans) (anurans) (anurans)

Amphibian Amphibian Duttaphrynus Duttaphrynus Leptodactylus labyrinthicus melanostictus melanostictus Rhinella marina Rhinella marina Rhinella marina

(snake) (lizard)

(snake) (snake)

(snake) (snake) (snake) (snake) (snake) (snake) Reptiles Borikenophis graueri Polemon fulvicollis Micrurus altirostrisMicrurus altirostrisMicrurus altirostrisMicrurus Apostolepisassimilis portoricensis Micrurus dissoleucusMicrurus Micrurus nigrocinctusMicrurus Varanus indicus Echis pyramidum

(owl)

Birds Birds Megascops choliba

Mammals Mammals

. Scolecophidia predation records available in the literature and in Schalk and Cove (2018). (2018). Cove inand Schalk availableand records inliterature predation the Scolecophidia Scolecophidia Table 1. Scolecophidia predation records available in the literature and in Schalk and Cove (2018). Cove and Schalk in and literature the in available records predation Scolecophidia Liotyphlops Antillotyphlops platycephalus brongersmianus Amerotyphlops Indotyphlops braminus

Madatyphlops punctatus Madatyphlops beui Liotyphlops beui Liotyphlops albirostris Liotyphlops albirostris Liotyphlops brongersmianus Amerotyphlops brongersmianus Amerotyphlops Indotyphlops braminus Indotyphlops braminus Madatyphlops cuneirostris Madatyphlops cuneirostris Anilios guentheri Snake species Snake Unidentified Anomalepididae Typhlopidae Typhlopidae Table 1. Table The blind snake Trilepida koppesi as prey of armadillo Euphractus sexcinctus 51 Toledo and Marais, 2013 Toledo Marais, 2013 and Bautista, 1998 Polis, 1979 Polis,and 1982 McCormick Anderson, 1956 Anderson, 1956 Carreira-Vidal, 2002 2002 Carreira-Vidal, and Embert Reichle, 2003 et al., Watkins-Colwell 2006 Kalmbach, 1944 1954 Taylor, 1984 Greene, and Setser 2004 Goode, 1973 Greene, 1973 Vitt Hulse, and andMata-Silva 2011 Johnson, and Setser 2004 Goode, and Chavez-Martinez Ramirez- Martins,1996

()

(scorpion) (scorpion) Arthropod Arthropod Reference arizonensis Smeringurus mesaensis Hadrurus sp.

(anurans)

Amphibian Amphibian Leptodactylus labyrinthicus

(snake)

(lizard)

(snake) (snake) (snake) (snake) (snake) (lizard) Reptiles Reptiles Uranoscodon Aspidoscelis Aspidoscelis deppii Micrurus altirostrisMicrurus Hypsiglena torquata Hypsiglena torquata superciliosus Apostolepis multicincta Micrurus fulviusMicrurus Unidentified coral snake coral Unidentified snake Micruroides euryxanthus

Birds Birds (falcon) Micrastur Micrastur gilvicollis

(bat)

sp. Mammals Mammals (armadillo) (Procionids) Bassariscus Dasypus novemcinctus Antrozous pallidus Antrozous

sp. Continued. Epictia tenella Epictia tenella Epictia Renahumilis Renahumilis

Rena humilis Renahumilis Epictia tenella Epictia tenella Renadulcis Renadulcis Renadulcis Renadulcis Renahumilis Renahumilis Renahumilis Renahumilis Rena maxima Epictia munoai Epictia munoai Epictia striatula Snake species Snake Table 1. Table 52 Silara Fatima Batista et al. Vaz-Silva et al., 2003 2003 Vaz-Silva et al., Bernarde & Abe, 2010 Bernarde Abe, & et al., Spawls 2004 et al., Spawls 2004 et al., Spawls 2004 et al., Spawls 2004 et al., Spawls 2004 et al., Spawls 2004 2007 Quiroga et al., Claúdio 2017 et al., studyThis

Arthropod Arthropod Reference

(frog) (anurans)

Amphibian Amphibian Leptodactylus labyrinthicus Rhinella arenarum arenarum Rhinella

(snake)

(snake) (snake) Reptiles Reptiles Aparallactus capensis Atractaspis irregularis Atractaspis irregularis Bothropsatrox

(owl)

Birds Birds Athene cunicularia

(canid)

(canid) (canid) (genet) . .

sp Mammals Mammals (armadillo) Genetta Vulpes chama Euphractus sexcinctus Canis mesomelas Otocyon megalotis

sp. sp.

Continued. scutifrons Leptotyphlops scutifrons Leptotyphlops scutifrons Leptotyphlops scutifrons Leptotyphlops scutifrons Leptotyphlops scutifrons Siagonodon borrichianus Trilepida Trilepida koppesi Trilepida koppesi Epictia Leptotyphlops longicaudus Snake species Snake Table 1. Table The blind snake Trilepida koppesi as prey of armadillo Euphractus sexcinctus 53

(according IN No 03, de 01 de setembro de 2014). The References analysis of this stomach revealed an entire specimen of Adalsteinsson, S.A., Branch, W.R., Trape, S., Vitt, L.J., Hedges, S.B. Trilepida koppesi (SVL: 337mm; TL: 25mm, female) (2009): Molecular phylogeny, classification, and biogeography (Figure 1). In addition, contents of the armadillo stomach of snakes of the Family Leptotyphlopidae (Reptilia, ). also included termites [Isoptera, Rhinotermitidae (n = Zootaxa 2244: 1–50. 16) and Kalotermitidae (n = 4 individuals)]. The snake is Anacleto, T.C.S. (2007): Food Habits of Four Armadillo Species housed on Coleção Herpetológica do Instituto Butantan in the Cerrado Area, Mato Grosso, Brazil. Zoological Studies 46(4): 529–537. (IBSP 91.417). Anderson, J.D. (1956): A blind snake preyed upon by a scorpion. Armadillos feed mainly on ants and termites, but they Herpetologica 12: 327. may also eat others small , carrion and some Arévalo-Páez, M., Montes-Correa, A.C., Rada-Vargas, E., Sabóya- fruit or other types of vegetal matter (Emmons and Feer, Acosta, L.P., Renjifo, J.M. (2015): Notes on the diet of the Pigmy 1997). The yellow armadillo is a common species found Coral Snake Micrurus dissoleucus (Cope, 1860) in northern in savannah habitats in most of (Redford Colombia (Serpentes: ). Notes 8: 39–41. and Wetzel, 1985). Although insects are common in the Barbo, F.E. (2008): Composição, História Natural, Diversidade e Distribuição das Serpentes no Município de São Paulo, SP. diet of E. sexcinctus, vertebrates, and more specifically Master dissertation, Universidade de São Paulo, São Paulo. snakes, are not so frequent (Dalponte and Tavares- Bernarde, P.S., Abe, A.S. (2010): Hábitos alimentares de serpentes Filho, 2004; Anacleto, 2007). This species, unlike other em Espigão do Oeste, Rondônia, Brasil. Biota Neotropica 10(1): species of armadillos, excavates new burrows, preferring 167–173. them in detriments of old burrows (Redford and Wetzel, Borges, L.M., Rosa, C.M., Dri, G.F., Bertani, R. (2016): Predation 1985). This foraging behavior may favor the encounter of the snake Erythrolamprus almadensis (Wagler, 1824) by the of fossorial snakes such as T. koppesi (Anacleto, 2007). tarantula Grammostola quirogai Montes De Oca, D’Elía & Pérez-Miles, 2016. Herpetology Notes 9: 321–322. It is also possible that the snake was captured during Campbell, J.A., Lamar, W.W. (2004): The Venomous Reptiles of foraging activities in termite nests, since this snake the Western Hemisphere. Comstock Publishing Associates, species forages on ant larvae and termites (Sawaya et Ithaca and London. 1032pp. al., 2008), as well as the yellow armadillo. Carreira Vidal, S. (2002): Alimentación de los ofídios de Knowledge about the natural history of scolecophidians . Asociación Herpetológica Española, Monografias de is sparse, usually obtained in the description and/or Herpetología 6: 126p. revision of the taxon, or in specific studies on the natural Casper, G. (1985): Prey capture and stinging behavior in the Emperor Scorpion, Pandinus Imperator (koch) (scorpiones, history and ecology of snake assemblages (e.g. Passos ). The Journal of Arachnology 13: 277–283. et al., 2006; Sawaya et al., 2008). For this reason, we Chavez-Martinez, A., Ramirez-Bautista, A. (1998): Cnemidophorus compiled the Scolecophidia predation records available (Whiptail Lizards) Diet. Herpetological Review 29: 98–100. in the literature, using genera, families and the infraorder Cláudio, V., Beltrame, L., Maffei, F. (2017): First record of as keywords. In addition, we included records compiled predation on Trilepida sp. (Serpentes, Leptotyphlopidae) by by Schalk and Cove (2018). We obtained 63 records of Athene cunicularia (Strigiformes, Strigidae) in the Brazilian predation on scolecophidians. Squamata are the most Cerrado. Herpetology Notes 10: 429–431. Costa, H.C., Bérnils, R. (2018): Répteis do Brasil e suas Unidades frequent predators, followed by amphibians, mammals, Federativas: Lista de espécies. Herpetologia Brasileira 8(1): birds and (Table 1). Most of these predators 11– 57. share similarities in foraging by digging the substrate Costa, H.C., Assis, C.L., Werneck, H.A., Nunes, A.V., Feio, R.N. or entering into gallery or hole. Thus, they can find and (2009): Ataque de um falcão acauã (Herpetotheres cachinnans) eat scolecophidians occasionally when investigating the sobre a serpente boipeva ( merremii) na Mata Atlântica soil (Casper, 1985; Myers et al., 2019). On the other de Minas Gerais, sudeste do Brasil. Biociências 11(2): 171–173. hand, predators that do not search for prey underground, Dalponte, J.C., Tavares-Filho, J.A. 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Accepted by Anamarija Zagar