Anais da Academia Brasileira de Ciências (2018) (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201820170976 www.scielo.br/aabc | www.fb.com/aabcjournal A giant on the ground: another large-bodied Atractus (Serpentes: Dipsadinae) from Ecuadorian Andes, with comments on the dietary specializations of the goo-eaters snakes PAULO PASSOS1, AGUSTÍN SCANFERLA2, PAULO R. MELO- SAMPAIO1, JORGE BRITO3,4 and ANA ALMENDARIZ3 1Departamento de Vertebrados, Museu Nacional, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista, 20940-040 Rio de Janeiro, RJ, Brazil 2CONICET, Instituto de Bio y Geociencias del NOA (IBIGEO), 9 de Julio 14 (A4405BBB), 4405, Rosario de Lerma, Salta, Argentina 3Museo de Historia Natural, Instituto de Ciencias Biológicas, Escuela Politecnica Nacional, Av. Ladrón de Guevara, PB 17-01-2759, Quito, Ecuador 4Instituto Nacional de Biodiversidad, Calle Rumipamba 341 y Av. de los Shyris, PB 17-07-8976, Quito, Ecuador Manuscript received on December 4, 2017; accepted for publication on January 12, 2018 ABSTRACT Body-size is significantly correlated with the number of vertebrae (pleomerism) in multiple vertebrate lineages, indicating that somitogenesis process is an important factor dictating evolutionary change associated to phyletic allometry and, consequently, species fitness and diversification. However, the role of the evolution of extreme body sizes (dwarfism and gigantism) remains elusive in snakes, mainly with respect to postnatal ontogeny in dietary preferences associated with evolution of gigantism in many lineages. We described herein a new species in the highly diversified and species-rich genus Atractus on the basis of four specimens from the southeastern slopes of the Ecuadorian Andes. The new species is morphologically similar and apparently closely related to two other allopatric giant congeners (A. gigas and A. touzeti), from which it can be distinguished by their distinct dorsal and ventral coloration, the number of supralabial and infralabial scales, the number of maxillary teeth, and relative width of the head. In addition, we discuss on the ontogenetic trajectories hypotheses and dietary specializations related to evolution of gigantism in the goo-eaters genus Atractus. Key words: Atractus gigas, Atractus touzeti, dietary shift, goo-eater snakes, macrostomy, postnatal ontogeny. INTRODUCTION organismal function), being the key factor in generating ecological and genetic divergence Body-size is among the most important species (Peters 1983, LaBarbera 1986, Hanken and Wake attributes (depicting common ancestry and 1993, Nagel and Schluter 1998, Schluter 2000), Correspondence to: Paulo Passos and is also correlated with increasing of extinction E-mail: [email protected] / [email protected] risk (Vilela et al. 2014). As such, the allometric * Contribution to the centenary of the Brazilian Academy of change in time is a primary axis for diversification Sciences. of many lineages, and can be important for An Acad Bras Cienc (2018) 90 2 dictating niche parameters, creating reproductive strong body constriction (Henderson and Powell isolation, and structuring communities (Losos 2007). Although pleomerism has been established 1992, Nagel and Schluter 1998, Schluter 2000, as an effective process to the body size evolution Moen and Wiens 2008). Some lineages have in snakes (Lindell 1994), only more recently the experienced extreme, and often paradoxical—the correlation between body size and developmental occurrence of giant diggers when most of fossorial evolution (= somatic growth) of giant snakes was tetrapods tend to miniaturization, see Hanken and addressed using a phylogenetic framework (Meik Wake (1993)—evolutionary change in body size 2010, Head and Polly 2007, 2015). (gigantism and dwarfism) due to colonizing new regions such islands or deep seas, re-colonization On the other hand, snakes are gape-limited of mainland after mass extinctions, environmental predators that swallow their prey whole without shifts or stochastic evolutionary novelty (Bonnet mechanical reduction prior to prey ingestion, except et al. 2009 and references therein). The extrinsic for few very specialized Homalopsine snakes (see factors (selective) responsible for the evolution Jayne et al. 2002). As a rule, the basal lineages of of body size extremes in terrestrial vertebrates snakes (e.g., Scolecophidians and Henophidians) have been a recent topic of interest (Meik et al. occupying underground macrohabitats feed on 2010 and references therein), but the intrinsic small size prey, such as insects, earthworms and mechanisms (developmental) underlying body size tiny elongate vertebrates; while alethinophidian evolution still poorly understood and under dispute snakes developed extreme anatomical adaptations in the recent literature (Head and Polly 2015 and (macrostomy) to ingest prey with large cross- references therein). section area in relation to their head dimensions. Body size is significantly correlated with Remarkably, several clades of small cryptozoic number of vertebrae (pleomerism) in multiple macrostomatans reverse postnatal morphological vertebrate lineages (Alexander and Gans 1966, transformations correlated with gape increasing to Lindsey 1975, Lindell 1994, Müller et al. 2010, a phenotype constraining the diet to prey with low Head and Polly 2007), indicating that increasing cross-section area (Scanferla 2016). However, it not body segments in the course of somitogenesis plays clear how some lineages evolved and maintained an important role in body size evolution (Lindell gigantism while having diets specialized in prey 1994). Snakes show greater variability in vertebral with small size and low caloric value (Arnold number than other amniotes (Müller et al. 2010, 1993), as some mollusks and annelids in the case Head and Polly 2007). The axial regionalization of Neotropical goo-eaters snakes (e.g., the genus is reduced in snakes by expansion of expressions Atractus). domains for Hox genes that code for the dorsal Our aim in this study, beyond describing region of the vertebral column, suppressing a new giant species from southeastern slopes expression of a distinct cervical region (Cohn and of the Ecuadorian Andes, is to discuss some Tickle 1999) or, by contrast, there is a retention of aspects related to postnatal ontogeny and dietary standard vertebrate Hox domains with alteration specialization found in the highly diversified and of downstream expression that suppresses species-rich genus Atractus. development of distinct regions (Woltering 2012). Among snakes, gigantism is pronounced in the MATERIALS AND METHODS constrictor species of the families Boidae and Pythonidae, which forage through a sit-and-wait Specimens examined are deposited in the following strategy and kill their prey by asphyxia due to collections: División de Herpetología del Museo An Acad Bras Cienc (2018) 90 NEW GIANT ATRACTUS FROM ECUADORIAN ANDES 3 Ecuatoriano de Ciencias Naturales (DHMECN), the nearest 1 mm. Measurements and descriptions Instituto Nacional de Biodiversidad, Quito of paired cephalic scales are strictly based on the Ecuador; Museo de Historia Natural de la Escuela right side of head. We measure the head length Politécnica Nacional (MEPN), Quito, Ecuador; from tip of rostral scale to the end of the quadrate- Museo de Zoología, Pontificia Universidad mandibular joint, head width in the broadest Católica del Ecuador (QCAZ), Quito, Ecuador; and region and midbody diameter at mid-length of Fundación Herpetológica Gustavo Orcés (FHGO), SVL. Counts of body marks (blotches, spots, and Quito, Ecuador. Comparative material of Atractus dots), in some taxa, were performed separately on gigas and Atractus touzeti is listed in Appendix I, each side of the dorsum because these marks are while additional congeners examined are listed in not always transversally continuous or equivalent Passos et al. (2005), Passos et al. (2007a, b), Passos and Fernandes (2008), Passos and Arredondo along the sides of vertebral region. Herein, the term (2009), Passos et al. (2009a, b, c, d, e), Passos et “blotch” refers to broader (two or more scales long al. (2010a, b, c), Passos and Lynch (2011), Passos and wide) dorsal marks located on the vertebral and Prudente (2012), Passos et al. (2012), Prudente and paravertebral regions, the term “spot” refers to and Passos (2008, 2010), Passos et al. (2013a, b, small (less than two scales long and wide) marks c, d), Almeida et al. (2014), Salazar-Valenzuela throughout the dorsum or venter, whereas “dot” et al. (2014), Passos et al. (2016a, b), de Fraga et refers to any mark smaller than a scale. The color al. (2017), and Passos et al. (2017). We provide tones follow Köhler (2012). Sex was determined on the authorship and date only in the first mention of the basis of presence/absence of hemipenes verified each name. through a ventral incision at the base of the tail. We GEOGRAPHICAL DATA examined maxillae in situ under a stereomicroscopy, through a narrow lateromedial incision between the Coordinates of localities were acquired in the field supralabials and the maxillary arch. After removing with Global Positioning System devices (referenced tissues covering the maxillary bone, we counted to map datum WGS84), and by consulting data in teeth and empty sockets. We follow Passos et al. museum catalogues or databases. We refined, when (2009e) and Passos et al. (2010c) with respect to possible, the provenance of records