First Record of Micrurus Diana Roze, 1983 (Serpentes: Elapidae) For

istributio First record of Roze, 1983 (Serpentes: D Elapidae) for Brazil and extension of its distribution in 1* raphic g Bolivia, 3 with notes on morphological 2 variation 2 eo Matheus Godoy Pires , Darlan Tavares Feitosa , Ana Lúcia da Costa Prudente and Nelson Jorge da G n

o Silva Jr.

1 Museu de Zoologia da Universidade de São Paulo. Avenida Nazaré 481. CEP 04263-000. São Paulo, SP, Brazil. otes

N 2 Museu Paraense Emílio Goeldi, Laboratório de Herpetologia. Avenida Perimetral 1901, CP 399. CEP 66040-170. Belém, PA, Brazil. 3 Pontifícia Universidade Cató[email protected] de Goiás, Programa de Pós-Graduação em Ciências Ambientais e Saúde. Rua 232 n° 128, 3° andar, Área V, Setor Universitário. CEP 74605-140. Goiânia, GO, Brazil. * Corresponding author. E-mail: Abstract: Micrurus diana

is a rare coral snake species poorly represented in museum collections. Based on two recently identified specimens, we report its occurrence for the first time in Brazil andM. for diana the Bolivian Yungas, substantially extending its known range. In addition, we also extend the limits of its known morphological variation, based on examination of 11 specimens. Our findings revealed the need of a better characterization for , and the need of preservation efforts for this species and its habitat in Brazil.

Micrurus diana Roze, 1983 was described as a subspecies of M. frontalis (Duméril, Bibron and Duméril, Paulo, Brazil (IBSP); Field Museum of the Natural History, Chicago, United States (FMNH); Museu de Zoologia da 1854) based on five specimens from “vicinity of Santiago” Universidade de São Paulo, São Paulo, Brazil (MZUSP); (Serranía de Santiago – 18°15’57”Micrurus S, 59°43’34” diana was W, Museu de Historia Natural Noel Kempff Mercado, Santa 700 m above sea level [asl]), province of Chiquiticos, Cruz de la Sierra, Bolivia (NMKR); Senckenberg Museum departamento de Santa Cruz, Bolivia. of Frankfurt, Germany (SMF); and Zoologisches Museum originally diagnosed by the fusion of the anteriorM. frontalis black Hamburg, Germany (ZMH). The description of the cephalic ring of the first body triad to the black cephalic cap that scales and color pattern followed Roze (1996), Silva Jr. and covers the parietals and distinguished from Sites (1999), and Savage andMicrurus Slowinski diana (1992). The list of by having immaculate red rings. Later, the same author specimens examined is included in Appendix I. Our data elevated it to full species status (Roze 1994) and repeats includerecord for two Micrurus new records diana of . Micrurusthe same diagnosis, frontalis based on the same data (Roze, 1996). Overall, this publication reports the first known Silva Jr. and Sites (1999) revised the taxonomyM. diana of based the in Brazil, extensively increases complex and presented additional its known distribution range in Bolivia, and contributes data on the morphological variation of to provideMZUSP a 17475 better (Figure understanding 1): of the morphological on a larger series than the previous works (Roze 1983;et variation of this species based on a larger series. al1994; 1996), providing new data on its distribution and Adult male; snout-vent variation, and improving the taxon diagnosis. Harvey length (SVL) 1000.00 mm; tail length (TL) 52.00 mm; of. M.(2003) diana revised the Bolivian coral snakes, summarized head length (HL) 29.14 mm; 11 body triads and 1 2/3 the morphological variation found in fourM. diana specimens triads on the tail; 214 ventral scales; and 21 subcaudal (NMKR 219,M. brasiliensis AMNH 120600, FMNH 195864 scales (Figures 1a and 1b). Dorsally, the head is black and FMNH 195899), and suggested that may (including rostral, internasals, prefrontals, frontal, and be synonymous with Roze, 1967, despite supraoculars) with white bordered scales; parietalsvs. their far allopatricM. diana distribution and M. brasiliensis (more than 1000 km). completely black (Figure 1c), anterior nd white supralabials ring of theare Campbell and Lamar (2004) compiled the available first triad narrower than the othersst rd(1 and dorsal 4 supralabials, scale 2 – information for keeping them 4 dorsal scales). Laterally, the 1 and 2 th as distinct species, although Gutberlet and Harvey (2004) white with black posterior border; 3 th th insisted to hypothesize the conspecificity between these nasal and preoculars black with white borders; 5 and 6 taxa on their conjectural “consensus phylogeny of coral supralabials, inferior postocular and temporals red withth snakes”. a brownish posterior border; superior postocular and 7 In order to confirm M.the diana identification of the specimens supralabial red with a black border (Figure 1d). Ventrally,nd mentioned in this paper, we used as comparative material the mental and first pair of infralabials are red with small eleven specimens of , including the complete irregularth black markings on the posterior borders; 2 type-series, housed in the following herpetological to 5 thpair of infralabials and anterior genials completely collections: American Museum of the Natural History, red; 6 pair of infralabials and posterior genials with the

New York, United States (AMNH); Instituto Butantan, São posterior black tips as part of the anterior black ring1556 of Pires et al. | First record of Micrurus diana for Brazil

th the first body triad, that includes the 7 infralabials, gular white and red rings of the same length and both a little scales and the first preventrals (Figure 1e). th longer than the black rings, keeping the characteristics of This specimen was collected on May 19 2008, within immaculate red rings and black tipped white scales. the drainage basin of the Parecis hydroelectric power We identifiedElaps thismarcgravii specimen during a visit to the plant reservoir (PCH Parecis), in the municipality of Zoologisches Museum Hamburg (Germany), previously Sapezal (13°4’30.21” S, 58°58’35.29” W, 345 m asl; Figure identifiedth as . It was collected by V. Rolle 2), western Mato Grosso, in the Juruena river basin, about on 28 May, 1897, in Charopampa, departamento de La 750 km north from the type-locality and 260 km northeast Paz, northwestern Bolivia (15°39’0.00” S, 67°55’0.00” fromZMH-R the nearest2704a (Figure record 3 (NMKR 219 of Serranía de W, 749 m asl; Figure 2). This record expands the known Huanchaca, Santa Cruz, Bolivia). distribution of the species about 850 km west-northeast ): Adult male: SVL 760.0 mm; from the type-locality and 550 km from the nearest known TL 62.4 mm; HL 20.5 mm; 12 body triads and 1 2/3 on record (IBSP 31342) from Jardín Botánico, Santa Cruz de the tail; 217 ventral scales; 27 subcaudal scales (Figure La Sierra. 3a, b). Dorsally, it has white bordered black cephalic scales MicrurusThe sample diana of 11 specimens analyzed in this work (including rostral, internasals, frontal, and supraoculars); (Appendix 1) not only expands the known distributionM. diana can of prefrontals irregularly marked with black; parietals , but also expands the variation range of black with red lateral and medial borders (Figure 3c). some diagnostic͞x characters♂ for the species.͞x ♀ 1Anterior nd white ring of the first triad is narrower than have 214 (MZUSP͞x 17475) to 237 (IBSP 31342, SMF 86637) thest others (2.5 dorsal scales).rd Laterally, it presents the ventral scales [ = 223.64͞x ( : 214 –♂ 223, = 217.67)͞x ( : and 2 supralabials, nasal and preoculars white with (223♀ – 237, ͞x = 230.8)]; 18 (FMNH 195899) to 27 (ZMH-R black posterior borders;th 3 supralabials black with whiteth 2704a) subcaudal scales [ = 22.09 ( : 21 – 27, ͞x = 23.17) anteriorth border and 4 supralabials completely black; 5 (♂: 18 – 23,͞x = 20.8)];♀ 9 (FMNH 195886, 195889, 195889,♂ and 6 supralabials and temporals red with black posterior AMNH 120600) to♀ 15 (SMF 86637) body triads [ = 10.55 border (Figure 3d); inferiorth postocular completely black; : 9 – 12, = 10) ( : 9 – 15)] and 1 to 1 2/3 tail triads [( : superior postocular and 7 supralabials rd red with pair black of 1 1/3 – 1 2/3) ( : 1 – 1 2/3)]. Red rings of the body can borders. Ventrally, the mental is black and the th first pair present all range between 3 (ZMH-R 2704a, SMF 86637) of infralabials red with black borders; 3 to 5 th to 13 scales in length (often with immaculate scales, but infralabials and first pair of genials completely red; 6 some degree of black-tipping or irregular black scales can of infralabials and second pair of genials red with posterior be present); white rings present all range between 2 (SMF tip covered by the black colorationth of the first ring of the 86637) to 5 (FMNH 195889) scales in length; the reduced first triad, including the 7 pair of infralabials, gulars, and anterior black ring of the first triad (fused with parietals) preventral scales (Figure 3e). This specimen presents often have 2 scales in length (3 scales in ZMH-R 2704a);

Figure 1. Micrurus diana

General view of (MZUSP 17475) (SVL: 1000 mm; TL: 52 mm): a) dorsal view of body; b) ventral view of body; c) dorsal view of head; d) lateral view of head; e) ventral view of head (Photos: Paola M. Sánchez Martínez). 1557 Pires et al. | First record of Micrurus diana for Brazil

rd and M. diana 4 vs M. diana nasalsth divided by nostril opening; 7/7 supralabials, 3 can be differentiated fromM. surinamensis by its tricolor monadal in contact with the orbit; one preocular;st th 2 postoculars; pattern ( . tricolor triadal pattern in ) (Savageth temporals 1+1; 7/7 infralabials (1 to 4͞x in contact with and Slowinski 1992); having only the 4 the anterior genials); anal scale divided. Snout-vent͞x length supralabials scales in contact withvs the orbit, black middle varying from 573–1000 mm in males ( = 804.7; SD = ring of the triads wider thanrd and the 4 external ones and black (157.6;͞x n = 7) and 484–925 mm in females ( = 673.5; SD = bordered red cephalic scales ( th. white bordered blackM. 209; n = 4); tail͞x length varying from 42–62.4 mm in males dianacephalic M.scale lemniscatus coloration, helleri3 supralabials in contact = 51.7; SD = 7; n = 7) (4.9–7.2% of total length) and from with the orbit, black triad rings of the same length in mm32–52.3 in males mm (͞x = 40.3; SD = 9.1; n = 4) (5.2–6.2% of total ); by the completely black length) in females. Head length varying͞x from 20.5–29.1 snout followed by a transversal white band through the = 23.9; SD = 3.5; n = 7) (2.7–3.6% of SVL) (prefrontalsvs and the first triad separated from the black and from 16 – 26.3 mm in females ( = 21.5; SD = 4.9; n = cephalic band by a wide red ring and black infralabials 4) (2.8–3.6%Micrurus of SVL). frontalis (Duméril, Bibron and Duméril, . the presence of a black and whiteM. snout, diana absenceM. spixii of Five speciesM. lemniscatus of coral snakes helleri are known to occur in Mato amartiusi transversal prefrontal white band, black cephalic band Grosso:M. paraensis M. spixii fused with the first black body ring in ); martiusi1854); M. surinamensis (Schmidt and Schmidt, by the vsfirst body triad composed by only two black 1925); Cunha and Nascimento, 1973; rings and separated from the black cephalicM. diana coloration Schmidt, 1953 and Micrurus (Cuvier, paraensis 1817) M.by frontalisa red ring ( . first triad fused with the black cephalic (Strüssmann and Sazima 1993; Carvalho and Nogueira coloration, higher number of body triads in ); and 1998; Strüssmann and Carvalho 1998). by the absence of fusion of the cephalic black

Figure 2. Micrurus diana

Known distribution of . Star: type locality; white circles: new records; black circles: previously known records.et 1)al. Bolivia, Santa Cruz, Serranía de Santiago; 2) Bolivia, Santa Cruz, Sansaba; 3) Bolivia, Santa Cruz, Santa Cruz de la Sierra; 4) Bolivia, Santa Cruz, San Sebastián; 5) Bolivia, Santa Cruz, Serranía de Huanchaca; 6) Bolivia, La Paz, Charopampa; 7) Brazil, Mato Grosso, Sapezal. Ecoregions following Olson (2001). 1558 Pires et al. | First record of Micrurus diana for Brazil

Figure 3. Micrurus diana

General view of (ZMH-R 2704a) (SVL: 760.0 mm; TL: 62.4 mm): a) dorsal view of body; b) ventral view of body; c) dorsal view of head; d) lateral view of head; e) ventral view of head (Photos: D. T. Feitosa). cap with the anterior black ringvs of the first triad , white a locality condemned to be flooded due to the installation rings longer than black rings on the body and usually a of a private hydroelectric powerplant of low performance higher number of body triads ( . black cephalic capM. diana fused) (PCH). This region is a very active front of natural landscape with the first black body ring, white rings longer than black substitution. The Cerrado is considered a hotspot of ringsMicrurus and lower diana mean number of body triads in biodiversity, having only 8.21% of its natural area under (Campbell and Lamar 2004; Silva Jr. and Sites 1999). “legal protection” (MMA,M. diana 2013), which by no means assure is a rare species of coral snake with few effective protection to its species, M.and diana what raises concern available material on zoological collections, consequently on the survival of in the Brazilian territory. All supported by weak diagnosis based on a poorly but ZMH-R 2704a specimens of were collected understood morphological variation. Our data reveals that in landscapes covered by open stands of vegetational the previously known variation boundaries on length and structure. The entire type series comes from the Dry appearance of red and white rings, and number ofM. triads frontalis for Chaco (MZUSP 17475), Cerrado (NMKR 219), and from this species were underestimated. The overlap on ventral Chiquitania (NMKRM. diana 4253 and IBSP 31342). The specimen and subcaudal numbers among ettaxa al. within the ZMH-R 2704a, fromet al. the Bolivian Yungas, represents the species complex is very common, as previously noted (Silva first record of in the forested habitats (ecoregions Jr. and Sites 1999; Di-Bernardo 2007). It is important followingAcknowledgments Olson : 2001). to remember that the diagnosis developed exclusively We are indebted to Martin Jansen (Senckenberg based on external features are often subject to revision, Museum) for granting us permission to examine the NMKR 4253 and internal characters such as skull and hemipenial specimen under his care at SMF and the curators and staff of the visited collections. We thank Jack W. Sites Jr., Jean M. Lawrence, Davi morphology mustM. frontalis be taken into account. On the presence Pantoja and Henrique Caldeira for revisions of this manuscript. We also of fused black cephalic caps with anterior ringset al. of the thank Systema Naturae Consultoria Ambiental Ltda., Coordenação de first triad in , what was stated by Roze (1983) Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (ALCP, and repeated by other authors (see Harvey 2003;M. process 308950/2011-9) (ALCP, PROTAX project 562171/2010-0) for frontalisCampbell and Lamar 2004), there is no strongM. evidence frontalis Literatureproviding financial Cited and logistical support. to associate this character to the presently recognized The Venomous Reptiles of Western Hemisphere . We are aware of only two specimens of Campbell, J.A. and W.W. Lamar. 2004. (MNHN 0.1484 from Caraça, Minas Gerais, and SMF 54734 . Vols. 1 & 2. Ithaca and London: Cornell University Press. from São Paulo, both in Brazil) with fusion of the black 962 p. Carvalho,Cadernos M.A. de and Saúde F. Nogueira. Pública 1998. Serpentes da área urbana de Cuiabá, cephalic cap with the anterior black ring of the first triad, Mato Grosso: aspectos ecológicos e acidentes ofídicos associados. based on expressive sample of 603 specimens. Therefore,M. Micrurus 14(4): 753-763. Zootaxa frontalisfused cephalic cap and M.white diana. rings longer than black rings Di-Bernardo, M., M. Borges-Martins and N.J. Silva Jr. 2007. A new species of coralsnake ( : Elapidae) from southern Brazil. of the triads at mid-dorsum are not fixed characters in 1447: 1-26. In as they are in GutberletThe Venomous Jr., R.L. andReptiles M.B. of Harvey. the Western 2004. Hemisphere. The Evolution of New World The state of Mato Grosso corresponds to 10.6% of the Venomous Snakes; p. 634-682 J.A. Campbell and W.W. Lamar (ed.). Volume II. Ithaca: Brazilian territory, covered by et portions al. of three major Comstock Publishing Associates. Micrurus Micrurusvegetational diana domains in South America: Amazonia, Harvey,Annals B.H., of E.J. the Aparicio Carnegie and Museum L. Gonzalez. 2003. Revision of the venomous Pantanal and Cerrado (Olson 2001). We found snakes of Bolivia: Part 1. The Coral Snakes (Elapidae: ). 72(1): 1-52. in the western Mato Grosso (Cerrado), in 1559 Pires et al. | First record of Micrurus diana for Brazil

O Bioma Cerrado. Herpetological Review MMA 2013. Eletronic document acessible at http:// Strüssmann, C. and M.A. Carvalho. 1998. New herpetological records for www.mma.gov.br/biomas/cerrado. Captured in 08 june 2013. Mato Grosso State, western Brazil. 29(3): 183- Olson, D.M., E. Dinerstein, E.D. Wikramanayake, N.D. Burgess, G.V.N. Powell, 185. E.C. Underwood, J.A. D’Amico, I. Itoua, H.E. Strand, J.C. Morrison, C.J. Loucks, T.F. Allnutt, T.H. Ricketts, Y.Bioscience Kura, J.F. Lamoreux, W.W. Wettengel, P. Hedao and K.R. Kassem. 2001. Terrestrial ecoregions of the world: a new mapMemórias of life ondo InstitutoEarth. Butantan 51(11): 933-938. Received: February 2013 Roze, J.A. 1983. New World Coral snakes (Elapidae): A taxonomic and Accepted: October 2013 biological summary.Bulletin of the Maryland Herpetological 46: Society 305-338. Published online: December 2013 Roze, J.A. 1994. Notes Taxonomy of venomous Coral Snakes (Elapidae) of Editorial responsibility: Davi L. Pantoja South America.Coral Snakes of the Americas – Biology, Identification, 30(4): and Venoms177-185. Roze, J.A. 1996. . Malabar: Krieger Publishing Co. 328 p. Appendix 1. Savage, J.M. and J.B. Biological Slowinski. Journal 1992. Theof Linnean coloration Society of the venomous Type series: coral snakes (family Elapidae) and their mimicsMicrurus (families frontalis Aniliidae Analyzed material and Colubridae). Herpetological Monographs 45: 235-254. BOLIVIA: Santa Cruz: Serranía de Santiago: FMNH 195889 Silva Jr., N.J. and J.W. Sites. 1999. Revision ofMicrurus the brasiliensis complex (Holotype); FMNH 195864 (Paratype); FMNH 195899 (Paratype); AMNH (Serpentes: Elapidae). 13: 142-194. Additional120600 (Paratype); material: Sansaba, 10 km W of Santiago: FMNH 195886 Silva Jr., N.J. 2007.Revista Novas Estudos ocorrências de Roze, 1967 (Paratype). (Serpentes: Elapidae) em áreas de tensão ambiental no centro-oeste BOLIVIA: La Paz: Charopampa: ZMH-R 2704a brasileiro. 34(11/12): 931-956. (New record); Santa Cruz: San Sebastián, near Concepción: NMKR 4253, Strüssmann,Studies on C. Neotropical and I. Sazima. Fauna 1993. and The Environment snake assemblage of the Pantanal SMF 86637; Santa Cruz de la Sierra: IBSP 31342; Serranía de Huanchaca: at Poconé, Western Brazil: Faunal composition and ecology summary. NMKR 219. BRAZIL: Mato Grosso: Sapezal: PCH Parecis: MZUSP 17475 28: 157-168. (New record).

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