Natural History of the Rare and Endangered Snake Atractus Ronnie (Serpentes: Colubridae) in Northeastern Brazil
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Phyllomedusa 18(1):77–87, 2019 © 2019 Universidade de São Paulo - ESALQ ISSN 1519-1397 (print) / ISSN 2316-9079 (online) doi: http://dx.doi.org/10.11606/issn.2316-9079.v18i1p77-87 Natural history of the rare and endangered snake Atractus ronnie (Serpentes: Colubridae) in northeastern Brazil Cristiana Ferreira-Silva,1 Samuel Cardozo Ribeiro,2 Edna Paulino de Alcantara,1 and Robson Waldemar Ávila3 1Departamento de Parasitologia, Instituto de Biociências, Universidade Estadual Paulista, Campus de Botucatu. 18080-970, Botucatu, SP, Brazil. E-mail: [email protected]. 2Instituto de Formação de Educadores, Universidade Federal do Cariri. 63260-000, Brejo Santo, CE, Brazil. 3Departamento de Ciências Biológicas, Universidade Regional do Cariri, Campus do Pimenta. 63100-000, Crato, CE, Brazil. Abstract Natural history of the rare and endangered snake Atractus ronnie (Serpentes: Colubridae) in northeastern Brazil. The habitat use, activity period, sexual dimorphism, morphological variation, reproduction and diet composition of this fossorial and nocturnal snake are reported. The snakes were captured between 2008–2014 in the Chapada do Araripe in northeastern Brazil, and were collected by active visual searches, as well as in pitfall traps with drift fences. Although females are larger than males, the males have longer tails, and scale counts differ between the sexes. Reproduction is seasonal, occurring during the rainy season. Brood sizes rang from one to four eggs. Atractus ronnie preys on earthworms, in addition to ants (Crematogaster sp.) and insect larvae. Keywords: Cerrado, diet, sexual dimorphism, habits, reproduction. Resumo História natural da serpente rara e ameaçada de extinção Atractus ronnie (Serpentes: Colubridae) no nordeste do Brasil. O uso do habitat, período de atividade, dimorfsmo sexual, variações morfológicas, reprodução e a composição da dieta desta serpente fossória e noturna são relatados. As serpentes foram capturadas entre 2008–2014 na Chapada do Araripe, nordeste do Brasil, e foram coletadas por meio de busca ativa, bem como em armadilhas de queda com cerca guias. Embora as fêmeas sejam maiores que os machos, os machos têm caudas mais longas e as contagens das escamas diferem entre os sexos. A reprodução é sazonal, ocorrendo durante a estação chuvosa. O tamanho da ninhada variou de um a quatro ovos. A principal presa de A. ronnie são minhocas, além de formigas (Crematogaster sp.) e larvas de insetos. Palavras-chave: Cerrado, dieta, dimorfsmo sexual, hábito, reprodução. Received 13 September 2018 Accepted 23 April 2019 Distributed June 2019 Phyllomedusa - 18(1), June 2019 77 Ferreira-Silva et al. Introduction and dry forest (semideciduous forest), with Cerrado, Cerradão (xeromorphic semideciduous The Neotropical snake genus Atractus forest), and Carrasco phytophysiognomies at the Wagler, 1828 is remarkably diverse, having top (Tabarelli and Santos 2004). The climate is about 150 species distributed from Panama to tropical—i.e., wet and hot with a rainy season Argentina (Giraudo and Scrocchi 2000, Myers from December–May. The mean annual preci- 2003, Passos et al. 2018). The descriptions of pitation is 1090 mm3 and the mean temperature most species are based on only a few specimens is 24–26°C (IPECE 2016). (e.g., Passos and Fernandes 2008, Passos et al. We carried out feldwork monthly at two 2010) and data on natural history are scant, sites on the slopes of the Chapada do Araripe, in owing to the secretive habits of the snakes the municipality of Crato, Ceará state. The frst (cryptozoic and semi-fossorial) and localized site was Delvechia ranch (07°15'19'' S, 39°28'12'' endemism. This has contributed to the small W; datum WGS 84; 729 m a.s.l.) between March sample sizes reported by many authors (e.g., 2008 and February 2010. The second was the Martins and Oliveira 1993, Cisneros-Heredia Ecological Trail of the Clube Recreativo 2005, Sawaya et al. 2008, Barbo et al. 2011). Granjeiro (07°16'47.0'' S, 39°26'17.7'' W; datum Atractus ronnie Passos, Fernandes, and WGS 84; 691 m a.s.l.) between September 2011 Borges-Nojosa, 2007 is endemic to the Caatinga and August 2012 and January–December 2014. Biome where it inhabits highland marshes in These sites are located in a narrow band of the Brazilian state of Ceará (Guedes et al. humid forest within the boundaries of the Araripe 2014). The taxon was frst described for the Environmental Protection Area (APA Araripe; Serra de Baturité Mountains (Passos et al. Figure 1). 2007), but the range also includes the Ibiapaba and Araripe Plateaus (Loebmann et al. 2009). Data Collection Atractus ronnie is a federally threatened species, cataloged as Endangered (EN) (MMA We found the snakes by active, visual- 2014). In the Chapada do Araripe, A. ronnie is encounter searches by day and by night, and by found only in a narrow strip of rainforest on the pitfall traps with drift fences (Table 1). For slopes (Ribeiro et al. 2012). Biological data on specimens that we collected by active searches, the species are scarce, with little information we recorded the time of capture and the substrate available other than the original description on which the snake was frst seen. We took the (Passos et al. 2007). Herein, we provide data on specimens to the Laboratório de Herpetologia da substrate use, activity period, sexual dimorphism, Universidade Regional do Cariri, where they morphological variation, reproduction and diet were euthanized with an intraperitoneal injection of A. ronnie at the Chapada do Araripe in of sodium thiopental 50 mg/kg as per the permits northeastern Brazil. issued by the Comitê de Ética em Pesquisa of the Universidade Regional do Cariri. The specimens Materials and Methods were fxed with 10% formalin and preserved in 70% ethanol. Voucher specimens are deposited Study Area in the Coleção Herpetológica da Universidade Regional do Cariri (URCA-H 149–158, 6203– The Chapada do Araripe is located in three 6204, 10067, 10131–10132, 10261–10264, states (Ceará, Piauí, and Pernambuco) in 10266, 10271, 10540, 10606, 10608–10609, northeast Brazil (Lima et al. 2012). The altitude 10656, 11019–11020) and in the Coleção varies from 500–1100 m a.s.l. On the slopes, the Herpetológica da Universidade Federal de vegetation is humid forest (tropical cloud forest) Pernambuco (CHUFPE 99 and 100). Phyllomedusa - 18(1), June 2019 78 Natural history of the rare and endangered snake Atractus ronnie Figure 1. Study area in the Chapada do Araripe, Ceará state, northern Brazil. APA Araripe = Araripe Environmental Protection Area, FLONA Araripe = Araripe National Forest. Legend to Brazilian states: CE, Ceará; PB, Paraíba; PE, Pernambuco; PI, Piauí; RN, Rio Grande do Norte. Data Analysis also counted ventral and subcaudal scales and dorsal scale rows (in 3 regions of the body—i.e., We examined a total of 30 Atractus ronnie counted one head length from the neck, the middle (Figure 2). For each specimen we recorded the of the body and one head length from the cloaca) following morphometric variables with digital (Peters 1964). Males were considered calipers to the nearest 0.01 mm: snout–vent reproductively active if they possessed convoluted length (SVL); head length (HL); head width deferent ducts (Shine 1988). Females were (HW); head height (HH); and tail length (TL). We considered reproductively active if they possessed Phyllomedusa - 18(1), June 2019 79 Ferreira-Silva et al. Table 1. Details of sampling methods used in the collection of Atractus ronnie at Chapada do Araripe, northeastern Brazil between 2008 and 2014. Total Sampling Description of the Number specimens Locality Period days in Total effort protocol sampling method collected during study the field Mar 5 arrays (4 buckets Pitfall traps 1.200 March 2008 (N = 9); Delvechia 2008– 20L per array) Y with drift 60 buckets- Ranch Feb shape; 5 days, bi- fences day February 2010 (N = 1) 2010 monthly collection Sep March (N = 1); 2011– Active 1 day per mo; 1 hr 48 hr- 12 June (N = 1) in diet of Aug searches per day; 4 collectors collector Bothrops leucurus Ecological 2012 trail of Pitfall traps 5 arrays (8 buckets 14.600 January (N = 3); February the Club with drift 365 60L per array) straight buckets- (N = 5); May (N = 1); Recreativo fences line day December (N = 2) Granjeiro Jan–Dec 2014 October (N = 1); Active 4 days per mo/ 3 hr 288 hr- 48 November (N = 5); searches per day; 2 collectors collector December (N = 1) faccid oviducts, ovarian follicles in secondary and subcaudal scales in adults. To determine if vitellogenesis (> 4 mm long) or oviductal eggs there is a correlation between SVL and testicle (modifed from Shine 1988); the simultaneous volume and between SVL and egg volume, we presence of both vitellogenic follicles and eggs used the parametric correlation of Pearson. was considered evidence of production of more Descriptive statistical analyses used throughout than one clutch per season (Shine 1977, Fitch the paper include means followed by ± SD. We 1982). We recorded the number of eggs and/or conducted all tests with 1.26 PAST software follicles, as well as the lengths and widths of (Hammer et al. 2001), using a 5% signifcance eggs, follicles, and testicles, and estimated their level. volumes using the ellipsoid formula: V = (4π/3) We dissected each specimen and analyzed (W/2)2(L/2), in which W and L represent width stomach contents, identifying the prey to the and length, respectively (e.g., Sousa and Ávila most precise taxonomic category possible. 2015). We calculated the sexual size dimorphism Results index (SSD) following Shine’s (1994) method in which the mean body size of the larger sex is Substrate Use and Activity Period divided by the mean body size of the smaller sex, minus one. Positive values represent females During active searches we observed eight larger than males, and negative values represent individual Atractus ronnie.