BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Taxonomic Status And Geographic Variation Of The Slender Coralsnake, Micrurus Filiformis (Günther, 1859) (Serpentes, Elapidae) Author(s): Darlan Tavares Feitosa, Paulo P. Passos, Ana Lúcia da Costa Prudente Source: South American Journal of Herpetology, 2(3):149-156. 2007. Published By: Brazilian Society of Herpetology DOI: http://dx.doi.org/10.2994/1808-9798(2007)2[149:TSAGVO]2.0.CO;2 URL: http://www.bioone.org/doi/full/10.2994/1808-9798%282007%292%5B149%3ATSAGVO %5D2.0.CO%3B2 BioOne (www.bioone.org ) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use . Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder.
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BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors nonprofit publishers academic institutionsresearch libraries and research funders in the common goal of maximizing access to critical research
Taxonomic Status And Geographic Variation Of The Slender CoralsnakeMicrurus Filiformis (Guumlnther 1859) (Serpentes Elapidae)Author(s) Darlan Tavares Feitosa Paulo P Passos Ana Luacutecia da Costa PrudenteSource South American Journal of Herpetology 2(3)149-156 2007Published By Brazilian Society of HerpetologyDOI httpdxdoiorg1029941808-9798(2007)2[149TSAGVO]20CO2URL httpwwwbiooneorgdoifull1029941808-97982820072925B1493ATSAGVO5D20CO3B2
BioOne (wwwbiooneorg) is a nonprofit online aggregation of core research in the biological ecologicaland environmental sciences BioOne provides a sustainable online platform for over 170 journals and bookspublished by nonprofit societies associations museums institutions and presses
Your use of this PDF the BioOne Web site and all posted and associated content indicates your acceptance ofBioOnersquos Terms of Use available at wwwbiooneorgpageterms_of_use
Usage of BioOne content is strictly limited to personal educational and non-commercial use Commercialinquiries or rights and permissions requests should be directed to the individual publisher as copyright holder
South American Journal of Herpetology 2(3) 2007 149-156copy 2007 Brazilian Society of Herpetology
TAXONOMIC STATUS AND GEOGRAPHIC VARIATION OF THE SLENDER CORALSNAKE MICRURUS FILIFORMIS
(GUumlNTHER 1859) (SERPENTES ELAPIDAE)
DARLAN TAVARES FEITOSA13 PAULO P PASSOS2 AND ANA LUacuteCIA DA COSTA PRUDENTE1
1 Coordenaccedilatildeo de Zoologia Laboratoacuterio de Herpetologia Museu Paraense Emiacutelio Goeldi Avenida Perimetral nordm 1901Caixa Postal 399 CEP 66017-970 Terra Firme Beleacutem Paraacute Brazil
2 Departamento de Vertebrados Museu NacionalUFRJ Quinta da Boa Vista sn Satildeo Cristoacutevatildeo Rio de Janeiro RJCEP 20940-040 Brazil
3 Corresponding author E-mail dtfeitosayahoocombr
ABSTRACT The taxonomic status of Micrurus filiformis is reevaluated employing a statistical framework Micrurus filiformis subtil-is is maintained in the synonymy of M filiformis based on the results of quantitative and qualitative analyses Further geographical variation of meristic morphometric and hemipenis characters are described The holotype of Micrurus filiformis is redescribed
synonymy of M f subtilis with the nominal race However Roze (1982) Perez-Santos and Moreno (1988) as well as Campbell and Lamar (1989) contin-ued to render this form a subspecific rank Later Roze (1996) followed the synonymyzation proposed before by Cunha and Nascimento (1982) showing variation of the number of ventral scales between populations of M filiformis from western and eastern Amazonia
Micrurus filiformis is widely distributed in the Amazonian rainforest occurring from Colombia to Peru in lowlands of the eastern versant of the Andesand in central and eastern Brazilian Amazonia (Camp-bell and Lamar 2004) In sharp contrast with the ex-tensive range of distribution M filiformis was report-ed only from a few specimens (see Roze 1996 and Campbell and Lamar 2004) Although M f subtilishas been synonymyzed with the nominal species the taxonomic status of the latter form was never evalu-ated at a populational level using a statistical frame-work Currently all samples used by different authors that either do or do not recognize M f subtilis were limited and generally did not include the analyses of the type series Furthermore M filiformis has a dis-junct distribution pattern with a large sampling gap between the westerneastern distribution extremes in the Upper Amazon Basin (see map 13 in Campbelland Lamar 2004)
The focus of this study is to reevaluate the taxonom-ic status of Micrurus filiformis with an analysis of a larger sample size now available in herpetological col-lections applying qualitative and quantitative methods We also describe the geographic variation concerning meristic morphometric and hemipenis characters
INTRODUCTION
The New World coralsnake genus Micrurus is currently recognized as a monophyletic group oc-curring from southeastern United States to southern South America (Slowinski 1995 Campbell and La-mar 2004) Roze (1996) provided a comprehensive taxonomic revision of the genus recognizing about 60 species Nevertheless the status of several species and subspecies should be reevaluated using a larger num-ber of specimens which could improve the statistical support for their recognition (Wiens and Servedio 2000 Passos and Fernandes 2005)
Guumlnther (1859) described Elaps filiformis based on a specimen from the State of Paraacute northern Brazil differing from the previously recognized species by the very slender body high number of ventral scales and pattern of triads Boulenger (1896) and Gomes (1918) reported some variation in meristic characters and number of triads for the species Amaral (1925) relocated Elaps filiformis to the genus Micrurus Roze (1967) described Micrurus filiformis subtilis on the basis of four specimens from southeastern Colombia near the brazilian border differing from the nominal species by having two postoculars and 274-279 ven-tral scales in male specimens (vs single postocular and 283-309 in females of M f filiformis) Dixon and Soini (1977) reported some variation on the number of postocular scales in M f subtilis from Iquitos re-gion Peru Subsequently Cunha and Nascimento (1982 1993) found interpopulational variation in the number of postocular scales and cephalic color pat-tern in specimens from eastern Paraacute suggesting the
150 Taxonomic status of Micrurus filiformis
MATERIAL AND METHODS
The study was based on 42 specimens from the following institutions Brazil ndash Instituto Butantan (IBSP) Satildeo Paulo SP Instituto Nacional de Pesqui-sas da Amazocircnia (INPA) Manaus Amazonas MuseuNacional do Rio de Janeiro (MNRJ) Rio de Janeiro RJ Museu Paraense Emiacutelio Goeldi (MPEG) Beleacutem Paraacute Colombia ndash Instituto de Ciencias Naturales(ICN) Universidad Nacional de Colocircmbia Bogotaacute DC Museo de la Salle (MLS) Universidad de la Salle Bogotaacute DC Cundinamarca England-NaturalHistory Museum (NHM) London Acronyms citation follows Leviton et al (1985) Specimens and locali-ties are listed in the Appendix
Meristic and morphometric data of the holotype of Micrurus filiformis were taken by Dr C McCarthy (NHM) but we also analyzed the color pattern and head plates of the holotype based on digital photographs
Observed characters are related to external mor-phology coloration and hemipenis The method used for counting ventral scales followed Dowling (1951) Color pattern description followed Savage and Slow-inski (1992) and Roze (1996) Techniques for hemi-penis preparation followed Manzani and Abe (1988) and Pesantes (1994) with the modifications proposed by Zaher and Prudente (1999 2003) Terminology for hemipenis description followed Slowinski (1995) and Roze (1996) Sex was determined by visual inspec-tion of relative tail length and girth Measurementswere taken with a dial caliper to the nearest 01 mmexcept for total length (TL) snout vent length (SVL)tail length (TAL) and head length (HL) which were measured with a flexible ruler to the nearest 1 mmFor the purpose of statistical analysis we recorded for each specimen 27 quantitative external morphologi-cal characters (6 meristic and 21 morphometric car-acters Table 2)
We employed an analysis of variance (ANOVA)using segmental counts to assess the presence or ab-sence of sexual dimorphism within each group and the whole sample We evaluated the assumptions of univariate normality and homocedasticity with the Kolmogorov-Smirnov and Levene tests respectively (Zar 1999) In cases where characters showed insuf-ficient variation to justify these assumptions we per-formed non-parametric tests such as Mann-Whitneyand Kruskal-Wallis (Zar 1999) We performed a prin-cipal components analysis (PCA) at group level to evaluate differentiation between the groups without a priori definition (Manly 2000) We projected the first two principal components onto orthogonal axes and
computed 95 confidence regions from the simula-tion of 1000 pseudoreplicate data matrices obtained by parametric bootstrap All principal-components loadings are portrayed as correlation vectors (direc-tional cosines) which are estimated for each charac-ter by correlations with projection scores across indi-viduals (Strauss 1985 Passos et al 2005)
We performed all computations using the software MATLAB 42c1 (MathWorks 1994) except normal-ity and homocedasticity tests and graphs for which we used STATISTICA 60 (Statsoft 2003)
RESULTS
Statistical analysis
Micrurus filiformis shows no significant sexual di-morphism in the morphometric and meristic charac-ters considered and therefore males and females were treated jointly in all subsequent analyses performed
Non-parametric (Mann-Whitney test) comparisons between groups showed no significant differences among populations representing both subspecies The projections of the bivariate plots based on scores of principal components analyses (Figure 1A) were un-able to discriminate the groups Some discrimination occurred mainly in the second principal component axis which was strongly correlated with the number of subcaudal scales (Figure 1B)
Systematic Account
Micrurus filiformis (Guumlnther 1859)Figures 2 and 3 Tables 1 and 2
Holotype ndash Adult male NHM 194612013 (formerly BMNH 194612013) from State of Paraacute Brazil
Feitosa DT et al 151
Diagnosis ndash Micrurus filiformis can be distinguished from all congeners by having the following com-bination of characters (1) slender body (diameter gt 5 mm) (2) black snout with a white band above internasals prefrontals and first two pairs of supral-abials (3) black band over most frontal and parietal shields (4) red gular scales (5) genials and first four pairs of infralabials uniformly black (6) 11-23 body triads (7) no supra-anal tubercles (8) ventral scales 270-316 in males and 275-333 in females (9) sub-caudal scales 33-45 in males and 30-41 in females (Figures 2 and 3)
Comparisons ndash Regarding all short-tailed Micruruswith the color pattern composed of triads (Slowinski 1995) M filiformis differs from them by having a very slender body (diameter gt 5 mm) and high num-ber of body triads (11-23)
With respect to the Amazon species of Micru-rus M filiformis is sympatric with at least eight taxa
of triadal coralsnakes It can be distinguished from M hemprichii hemprichii and M h ortoni by having a divided cloacal plate (vs single) 11-23 body triads (vs 7-10 in M h hemprichii and 5-6 in M h ortoni)and by the absence of a cephalic black cap (vs black cap originated in the rostral plate running to the post-
FIGURE 1 (A) Bivariate plot with 95 confidence regions for the first 2 axes derived from scores of PCA analysis for populations of Micrurus filiformis (B) Correlations of meristic characters with corresponding principal components (directional cosines) Num-ber of ventral scales = 1 and number of subcaudal scales = 2
FIGURE 3 Dorsal body view of Micrurus filiformis in life (MPEG21760) SVL 460 mm and TAL 35 mm Photograph by G Mas-chio
FIGURE 2 Dorsal (A) ventral (B) and lateral (C) views of Micru-rus filiformis (MPEG 21760) Scale = 5 mm
152 Taxonomic status of Micrurus filiformis
orbital region) from M surinamensis and M nattereriby having third and fourth supralabials contacting the orbit (vs fourth only) diameter of body lt 5 mm (vsbody diameter gt 5 mm) and by reaching a maximum total length of 700 mm (vs maximum total length 900 to 1350) from M spixii spixii M s martiusi and M s obscurus by the lack of a black cap (vs black cap from rostral to frontal plate) and by reaching a maximum total length of 700 mm (vs 1520 mm to 1600 mm maximum total length)
On the basis of general color pattern and hemipe-nial morphology Micrurus filiformis is traditionally placed in the Micrurus lemniscatus species group Re-garding the species currently comprising that group M filiformis is sympatric with M lemniscatus lem-niscatus M l diutius M l helleri and M isozonusbut differs from them by having a high number of ventrals subcaudals and triads throughout the body and tail (see Table 1 for additional diagnostic features of the Amazonian triadal coralsnakes)
Redescription of the holotype ndash Head slightly distinct from body 367 mm SVL 33 mm TAL rostral vis-ible from above about twice as high as wide nasal semidivided rostral as high as long preocular single about twice as long as high postocular single about twice as high as long temporals 1+1 anterior tem-poral twice as long as high prefrontal length slightly longer than internasal supraocular twice as long as wide frontal twice as long as wide parietals about twice the width of frontal seven supralabials third and fourth contacting orbit seven infralabiais first four in contact with the anterior pair of chinshields anterior chinshields twice as long as wide posterior chinshields three times as long as wide cloacal plate divided three preventrals 295 ventral and 44 subcau-dal scales
Snout black including rostral first pair of su-pralabials and anterior portions of internasals pale (creamish white) band covering second pair of supra-labial posterior portions of nasals and prefrontals black band covering third to fifth supralabials pre and post-oculars anterior temporal supraocular frontal and anterior portion of parietals black cephalic band followed by red ring on the neck originates over the sixth supralabial posteriorly covering the seventh su-pralabial posterior temporal and posterior portion of parietals until the second dorsal Twenty one tri-ads along the body with 67 black 45 pale (creamish white) and 22 red rings including the post-cephalic stripe first body triad with large black ring dorsally 18th triad formed by five black and four pale rings
(= pentads) tail with one-mid triad with five black three pale and two red rings
Color pattern variation (Figures 2 and 3) ndash Snout with rostral first pair of supralabials anterior portions of nasal internasals and anterior portions of prefrontals generally uniformly black (Figure 2) an irregular pale band usually covers the posterior portions of second and anterior part of third pairs of supralabials pre-frontals and anterior portions of preoculars a large black band originates at posterior half of third pair of supralabials running to the anterior part of sixth pair of supralabials anterior temporal frontal and anterior portions of parietals parietal region with red ring limited by first body triad (Figures 3A B and C)Males having 11+frac12 to 23 and females 13 to 21+frac12 triads along the body middle black ring generally (four to six dorsal and three to five ventral scales in length) longer than the external black rings (generally three to four dorsal scales in length) pale rings (two to four dorsal or three to five scales in length) gener-ally with apical portion of each scale black tipped red rings (three to seven dorsal and three to eight ventral scales in length) generally with apical portion of each scale black tipped eventually triads might collapse forming pentads composed by five black and four to five pale rings (N = 4 including the holotype) gular region with symphysial cleft first four pairs of in-fralabials and first chin shields uniformly black (Fig-ure 3) belly scattered with small black dots on the red rings (Figure 2)
Meristic and morphometric variation (Table 2) ndash Third to fourth (N = 40) or third to fifth (N = 2) su-pralabials contacting orbit postoculars 01 (N = 1)11 (N = 14) 21 (N = 5) and 22 (N = 16) tempo-rals 1+1 (N = 35) and 1+2 (N = 1) generally four gu-lar scales (scales between last infralabials and chin shields) generally four preventrals ventrals 235-323(x = 2901 SD = 229 N = 23) in males and 231-323(x = 2924 SD = 321 N = 9) in females subcaudals 36-45 in males (Mean = 408 SD = 23 N = 23) and 32-41 in females (x = 382 SD = 23 N = 10 see Table 2 for additional variation on the meristic and morphometric characters)
Hemipenis (Figure 4) ndash Inverted organ (in situ)four subcaudals long bifurcating at second subcaudal level everted and maximally expanded organ short slightly bilobed and capitate sulcus spermaticus deep bifurcating on the terminal third of the hemipe-nial body with centrolineal orientation lobes short ornamented by few spines and spinules capitular
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
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FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
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PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
South American Journal of Herpetology 2(3) 2007 149-156copy 2007 Brazilian Society of Herpetology
TAXONOMIC STATUS AND GEOGRAPHIC VARIATION OF THE SLENDER CORALSNAKE MICRURUS FILIFORMIS
(GUumlNTHER 1859) (SERPENTES ELAPIDAE)
DARLAN TAVARES FEITOSA13 PAULO P PASSOS2 AND ANA LUacuteCIA DA COSTA PRUDENTE1
1 Coordenaccedilatildeo de Zoologia Laboratoacuterio de Herpetologia Museu Paraense Emiacutelio Goeldi Avenida Perimetral nordm 1901Caixa Postal 399 CEP 66017-970 Terra Firme Beleacutem Paraacute Brazil
2 Departamento de Vertebrados Museu NacionalUFRJ Quinta da Boa Vista sn Satildeo Cristoacutevatildeo Rio de Janeiro RJCEP 20940-040 Brazil
3 Corresponding author E-mail dtfeitosayahoocombr
ABSTRACT The taxonomic status of Micrurus filiformis is reevaluated employing a statistical framework Micrurus filiformis subtil-is is maintained in the synonymy of M filiformis based on the results of quantitative and qualitative analyses Further geographical variation of meristic morphometric and hemipenis characters are described The holotype of Micrurus filiformis is redescribed
synonymy of M f subtilis with the nominal race However Roze (1982) Perez-Santos and Moreno (1988) as well as Campbell and Lamar (1989) contin-ued to render this form a subspecific rank Later Roze (1996) followed the synonymyzation proposed before by Cunha and Nascimento (1982) showing variation of the number of ventral scales between populations of M filiformis from western and eastern Amazonia
Micrurus filiformis is widely distributed in the Amazonian rainforest occurring from Colombia to Peru in lowlands of the eastern versant of the Andesand in central and eastern Brazilian Amazonia (Camp-bell and Lamar 2004) In sharp contrast with the ex-tensive range of distribution M filiformis was report-ed only from a few specimens (see Roze 1996 and Campbell and Lamar 2004) Although M f subtilishas been synonymyzed with the nominal species the taxonomic status of the latter form was never evalu-ated at a populational level using a statistical frame-work Currently all samples used by different authors that either do or do not recognize M f subtilis were limited and generally did not include the analyses of the type series Furthermore M filiformis has a dis-junct distribution pattern with a large sampling gap between the westerneastern distribution extremes in the Upper Amazon Basin (see map 13 in Campbelland Lamar 2004)
The focus of this study is to reevaluate the taxonom-ic status of Micrurus filiformis with an analysis of a larger sample size now available in herpetological col-lections applying qualitative and quantitative methods We also describe the geographic variation concerning meristic morphometric and hemipenis characters
INTRODUCTION
The New World coralsnake genus Micrurus is currently recognized as a monophyletic group oc-curring from southeastern United States to southern South America (Slowinski 1995 Campbell and La-mar 2004) Roze (1996) provided a comprehensive taxonomic revision of the genus recognizing about 60 species Nevertheless the status of several species and subspecies should be reevaluated using a larger num-ber of specimens which could improve the statistical support for their recognition (Wiens and Servedio 2000 Passos and Fernandes 2005)
Guumlnther (1859) described Elaps filiformis based on a specimen from the State of Paraacute northern Brazil differing from the previously recognized species by the very slender body high number of ventral scales and pattern of triads Boulenger (1896) and Gomes (1918) reported some variation in meristic characters and number of triads for the species Amaral (1925) relocated Elaps filiformis to the genus Micrurus Roze (1967) described Micrurus filiformis subtilis on the basis of four specimens from southeastern Colombia near the brazilian border differing from the nominal species by having two postoculars and 274-279 ven-tral scales in male specimens (vs single postocular and 283-309 in females of M f filiformis) Dixon and Soini (1977) reported some variation on the number of postocular scales in M f subtilis from Iquitos re-gion Peru Subsequently Cunha and Nascimento (1982 1993) found interpopulational variation in the number of postocular scales and cephalic color pat-tern in specimens from eastern Paraacute suggesting the
150 Taxonomic status of Micrurus filiformis
MATERIAL AND METHODS
The study was based on 42 specimens from the following institutions Brazil ndash Instituto Butantan (IBSP) Satildeo Paulo SP Instituto Nacional de Pesqui-sas da Amazocircnia (INPA) Manaus Amazonas MuseuNacional do Rio de Janeiro (MNRJ) Rio de Janeiro RJ Museu Paraense Emiacutelio Goeldi (MPEG) Beleacutem Paraacute Colombia ndash Instituto de Ciencias Naturales(ICN) Universidad Nacional de Colocircmbia Bogotaacute DC Museo de la Salle (MLS) Universidad de la Salle Bogotaacute DC Cundinamarca England-NaturalHistory Museum (NHM) London Acronyms citation follows Leviton et al (1985) Specimens and locali-ties are listed in the Appendix
Meristic and morphometric data of the holotype of Micrurus filiformis were taken by Dr C McCarthy (NHM) but we also analyzed the color pattern and head plates of the holotype based on digital photographs
Observed characters are related to external mor-phology coloration and hemipenis The method used for counting ventral scales followed Dowling (1951) Color pattern description followed Savage and Slow-inski (1992) and Roze (1996) Techniques for hemi-penis preparation followed Manzani and Abe (1988) and Pesantes (1994) with the modifications proposed by Zaher and Prudente (1999 2003) Terminology for hemipenis description followed Slowinski (1995) and Roze (1996) Sex was determined by visual inspec-tion of relative tail length and girth Measurementswere taken with a dial caliper to the nearest 01 mmexcept for total length (TL) snout vent length (SVL)tail length (TAL) and head length (HL) which were measured with a flexible ruler to the nearest 1 mmFor the purpose of statistical analysis we recorded for each specimen 27 quantitative external morphologi-cal characters (6 meristic and 21 morphometric car-acters Table 2)
We employed an analysis of variance (ANOVA)using segmental counts to assess the presence or ab-sence of sexual dimorphism within each group and the whole sample We evaluated the assumptions of univariate normality and homocedasticity with the Kolmogorov-Smirnov and Levene tests respectively (Zar 1999) In cases where characters showed insuf-ficient variation to justify these assumptions we per-formed non-parametric tests such as Mann-Whitneyand Kruskal-Wallis (Zar 1999) We performed a prin-cipal components analysis (PCA) at group level to evaluate differentiation between the groups without a priori definition (Manly 2000) We projected the first two principal components onto orthogonal axes and
computed 95 confidence regions from the simula-tion of 1000 pseudoreplicate data matrices obtained by parametric bootstrap All principal-components loadings are portrayed as correlation vectors (direc-tional cosines) which are estimated for each charac-ter by correlations with projection scores across indi-viduals (Strauss 1985 Passos et al 2005)
We performed all computations using the software MATLAB 42c1 (MathWorks 1994) except normal-ity and homocedasticity tests and graphs for which we used STATISTICA 60 (Statsoft 2003)
RESULTS
Statistical analysis
Micrurus filiformis shows no significant sexual di-morphism in the morphometric and meristic charac-ters considered and therefore males and females were treated jointly in all subsequent analyses performed
Non-parametric (Mann-Whitney test) comparisons between groups showed no significant differences among populations representing both subspecies The projections of the bivariate plots based on scores of principal components analyses (Figure 1A) were un-able to discriminate the groups Some discrimination occurred mainly in the second principal component axis which was strongly correlated with the number of subcaudal scales (Figure 1B)
Systematic Account
Micrurus filiformis (Guumlnther 1859)Figures 2 and 3 Tables 1 and 2
Holotype ndash Adult male NHM 194612013 (formerly BMNH 194612013) from State of Paraacute Brazil
Feitosa DT et al 151
Diagnosis ndash Micrurus filiformis can be distinguished from all congeners by having the following com-bination of characters (1) slender body (diameter gt 5 mm) (2) black snout with a white band above internasals prefrontals and first two pairs of supral-abials (3) black band over most frontal and parietal shields (4) red gular scales (5) genials and first four pairs of infralabials uniformly black (6) 11-23 body triads (7) no supra-anal tubercles (8) ventral scales 270-316 in males and 275-333 in females (9) sub-caudal scales 33-45 in males and 30-41 in females (Figures 2 and 3)
Comparisons ndash Regarding all short-tailed Micruruswith the color pattern composed of triads (Slowinski 1995) M filiformis differs from them by having a very slender body (diameter gt 5 mm) and high num-ber of body triads (11-23)
With respect to the Amazon species of Micru-rus M filiformis is sympatric with at least eight taxa
of triadal coralsnakes It can be distinguished from M hemprichii hemprichii and M h ortoni by having a divided cloacal plate (vs single) 11-23 body triads (vs 7-10 in M h hemprichii and 5-6 in M h ortoni)and by the absence of a cephalic black cap (vs black cap originated in the rostral plate running to the post-
FIGURE 1 (A) Bivariate plot with 95 confidence regions for the first 2 axes derived from scores of PCA analysis for populations of Micrurus filiformis (B) Correlations of meristic characters with corresponding principal components (directional cosines) Num-ber of ventral scales = 1 and number of subcaudal scales = 2
FIGURE 3 Dorsal body view of Micrurus filiformis in life (MPEG21760) SVL 460 mm and TAL 35 mm Photograph by G Mas-chio
FIGURE 2 Dorsal (A) ventral (B) and lateral (C) views of Micru-rus filiformis (MPEG 21760) Scale = 5 mm
152 Taxonomic status of Micrurus filiformis
orbital region) from M surinamensis and M nattereriby having third and fourth supralabials contacting the orbit (vs fourth only) diameter of body lt 5 mm (vsbody diameter gt 5 mm) and by reaching a maximum total length of 700 mm (vs maximum total length 900 to 1350) from M spixii spixii M s martiusi and M s obscurus by the lack of a black cap (vs black cap from rostral to frontal plate) and by reaching a maximum total length of 700 mm (vs 1520 mm to 1600 mm maximum total length)
On the basis of general color pattern and hemipe-nial morphology Micrurus filiformis is traditionally placed in the Micrurus lemniscatus species group Re-garding the species currently comprising that group M filiformis is sympatric with M lemniscatus lem-niscatus M l diutius M l helleri and M isozonusbut differs from them by having a high number of ventrals subcaudals and triads throughout the body and tail (see Table 1 for additional diagnostic features of the Amazonian triadal coralsnakes)
Redescription of the holotype ndash Head slightly distinct from body 367 mm SVL 33 mm TAL rostral vis-ible from above about twice as high as wide nasal semidivided rostral as high as long preocular single about twice as long as high postocular single about twice as high as long temporals 1+1 anterior tem-poral twice as long as high prefrontal length slightly longer than internasal supraocular twice as long as wide frontal twice as long as wide parietals about twice the width of frontal seven supralabials third and fourth contacting orbit seven infralabiais first four in contact with the anterior pair of chinshields anterior chinshields twice as long as wide posterior chinshields three times as long as wide cloacal plate divided three preventrals 295 ventral and 44 subcau-dal scales
Snout black including rostral first pair of su-pralabials and anterior portions of internasals pale (creamish white) band covering second pair of supra-labial posterior portions of nasals and prefrontals black band covering third to fifth supralabials pre and post-oculars anterior temporal supraocular frontal and anterior portion of parietals black cephalic band followed by red ring on the neck originates over the sixth supralabial posteriorly covering the seventh su-pralabial posterior temporal and posterior portion of parietals until the second dorsal Twenty one tri-ads along the body with 67 black 45 pale (creamish white) and 22 red rings including the post-cephalic stripe first body triad with large black ring dorsally 18th triad formed by five black and four pale rings
(= pentads) tail with one-mid triad with five black three pale and two red rings
Color pattern variation (Figures 2 and 3) ndash Snout with rostral first pair of supralabials anterior portions of nasal internasals and anterior portions of prefrontals generally uniformly black (Figure 2) an irregular pale band usually covers the posterior portions of second and anterior part of third pairs of supralabials pre-frontals and anterior portions of preoculars a large black band originates at posterior half of third pair of supralabials running to the anterior part of sixth pair of supralabials anterior temporal frontal and anterior portions of parietals parietal region with red ring limited by first body triad (Figures 3A B and C)Males having 11+frac12 to 23 and females 13 to 21+frac12 triads along the body middle black ring generally (four to six dorsal and three to five ventral scales in length) longer than the external black rings (generally three to four dorsal scales in length) pale rings (two to four dorsal or three to five scales in length) gener-ally with apical portion of each scale black tipped red rings (three to seven dorsal and three to eight ventral scales in length) generally with apical portion of each scale black tipped eventually triads might collapse forming pentads composed by five black and four to five pale rings (N = 4 including the holotype) gular region with symphysial cleft first four pairs of in-fralabials and first chin shields uniformly black (Fig-ure 3) belly scattered with small black dots on the red rings (Figure 2)
Meristic and morphometric variation (Table 2) ndash Third to fourth (N = 40) or third to fifth (N = 2) su-pralabials contacting orbit postoculars 01 (N = 1)11 (N = 14) 21 (N = 5) and 22 (N = 16) tempo-rals 1+1 (N = 35) and 1+2 (N = 1) generally four gu-lar scales (scales between last infralabials and chin shields) generally four preventrals ventrals 235-323(x = 2901 SD = 229 N = 23) in males and 231-323(x = 2924 SD = 321 N = 9) in females subcaudals 36-45 in males (Mean = 408 SD = 23 N = 23) and 32-41 in females (x = 382 SD = 23 N = 10 see Table 2 for additional variation on the meristic and morphometric characters)
Hemipenis (Figure 4) ndash Inverted organ (in situ)four subcaudals long bifurcating at second subcaudal level everted and maximally expanded organ short slightly bilobed and capitate sulcus spermaticus deep bifurcating on the terminal third of the hemipe-nial body with centrolineal orientation lobes short ornamented by few spines and spinules capitular
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
150 Taxonomic status of Micrurus filiformis
MATERIAL AND METHODS
The study was based on 42 specimens from the following institutions Brazil ndash Instituto Butantan (IBSP) Satildeo Paulo SP Instituto Nacional de Pesqui-sas da Amazocircnia (INPA) Manaus Amazonas MuseuNacional do Rio de Janeiro (MNRJ) Rio de Janeiro RJ Museu Paraense Emiacutelio Goeldi (MPEG) Beleacutem Paraacute Colombia ndash Instituto de Ciencias Naturales(ICN) Universidad Nacional de Colocircmbia Bogotaacute DC Museo de la Salle (MLS) Universidad de la Salle Bogotaacute DC Cundinamarca England-NaturalHistory Museum (NHM) London Acronyms citation follows Leviton et al (1985) Specimens and locali-ties are listed in the Appendix
Meristic and morphometric data of the holotype of Micrurus filiformis were taken by Dr C McCarthy (NHM) but we also analyzed the color pattern and head plates of the holotype based on digital photographs
Observed characters are related to external mor-phology coloration and hemipenis The method used for counting ventral scales followed Dowling (1951) Color pattern description followed Savage and Slow-inski (1992) and Roze (1996) Techniques for hemi-penis preparation followed Manzani and Abe (1988) and Pesantes (1994) with the modifications proposed by Zaher and Prudente (1999 2003) Terminology for hemipenis description followed Slowinski (1995) and Roze (1996) Sex was determined by visual inspec-tion of relative tail length and girth Measurementswere taken with a dial caliper to the nearest 01 mmexcept for total length (TL) snout vent length (SVL)tail length (TAL) and head length (HL) which were measured with a flexible ruler to the nearest 1 mmFor the purpose of statistical analysis we recorded for each specimen 27 quantitative external morphologi-cal characters (6 meristic and 21 morphometric car-acters Table 2)
We employed an analysis of variance (ANOVA)using segmental counts to assess the presence or ab-sence of sexual dimorphism within each group and the whole sample We evaluated the assumptions of univariate normality and homocedasticity with the Kolmogorov-Smirnov and Levene tests respectively (Zar 1999) In cases where characters showed insuf-ficient variation to justify these assumptions we per-formed non-parametric tests such as Mann-Whitneyand Kruskal-Wallis (Zar 1999) We performed a prin-cipal components analysis (PCA) at group level to evaluate differentiation between the groups without a priori definition (Manly 2000) We projected the first two principal components onto orthogonal axes and
computed 95 confidence regions from the simula-tion of 1000 pseudoreplicate data matrices obtained by parametric bootstrap All principal-components loadings are portrayed as correlation vectors (direc-tional cosines) which are estimated for each charac-ter by correlations with projection scores across indi-viduals (Strauss 1985 Passos et al 2005)
We performed all computations using the software MATLAB 42c1 (MathWorks 1994) except normal-ity and homocedasticity tests and graphs for which we used STATISTICA 60 (Statsoft 2003)
RESULTS
Statistical analysis
Micrurus filiformis shows no significant sexual di-morphism in the morphometric and meristic charac-ters considered and therefore males and females were treated jointly in all subsequent analyses performed
Non-parametric (Mann-Whitney test) comparisons between groups showed no significant differences among populations representing both subspecies The projections of the bivariate plots based on scores of principal components analyses (Figure 1A) were un-able to discriminate the groups Some discrimination occurred mainly in the second principal component axis which was strongly correlated with the number of subcaudal scales (Figure 1B)
Systematic Account
Micrurus filiformis (Guumlnther 1859)Figures 2 and 3 Tables 1 and 2
Holotype ndash Adult male NHM 194612013 (formerly BMNH 194612013) from State of Paraacute Brazil
Feitosa DT et al 151
Diagnosis ndash Micrurus filiformis can be distinguished from all congeners by having the following com-bination of characters (1) slender body (diameter gt 5 mm) (2) black snout with a white band above internasals prefrontals and first two pairs of supral-abials (3) black band over most frontal and parietal shields (4) red gular scales (5) genials and first four pairs of infralabials uniformly black (6) 11-23 body triads (7) no supra-anal tubercles (8) ventral scales 270-316 in males and 275-333 in females (9) sub-caudal scales 33-45 in males and 30-41 in females (Figures 2 and 3)
Comparisons ndash Regarding all short-tailed Micruruswith the color pattern composed of triads (Slowinski 1995) M filiformis differs from them by having a very slender body (diameter gt 5 mm) and high num-ber of body triads (11-23)
With respect to the Amazon species of Micru-rus M filiformis is sympatric with at least eight taxa
of triadal coralsnakes It can be distinguished from M hemprichii hemprichii and M h ortoni by having a divided cloacal plate (vs single) 11-23 body triads (vs 7-10 in M h hemprichii and 5-6 in M h ortoni)and by the absence of a cephalic black cap (vs black cap originated in the rostral plate running to the post-
FIGURE 1 (A) Bivariate plot with 95 confidence regions for the first 2 axes derived from scores of PCA analysis for populations of Micrurus filiformis (B) Correlations of meristic characters with corresponding principal components (directional cosines) Num-ber of ventral scales = 1 and number of subcaudal scales = 2
FIGURE 3 Dorsal body view of Micrurus filiformis in life (MPEG21760) SVL 460 mm and TAL 35 mm Photograph by G Mas-chio
FIGURE 2 Dorsal (A) ventral (B) and lateral (C) views of Micru-rus filiformis (MPEG 21760) Scale = 5 mm
152 Taxonomic status of Micrurus filiformis
orbital region) from M surinamensis and M nattereriby having third and fourth supralabials contacting the orbit (vs fourth only) diameter of body lt 5 mm (vsbody diameter gt 5 mm) and by reaching a maximum total length of 700 mm (vs maximum total length 900 to 1350) from M spixii spixii M s martiusi and M s obscurus by the lack of a black cap (vs black cap from rostral to frontal plate) and by reaching a maximum total length of 700 mm (vs 1520 mm to 1600 mm maximum total length)
On the basis of general color pattern and hemipe-nial morphology Micrurus filiformis is traditionally placed in the Micrurus lemniscatus species group Re-garding the species currently comprising that group M filiformis is sympatric with M lemniscatus lem-niscatus M l diutius M l helleri and M isozonusbut differs from them by having a high number of ventrals subcaudals and triads throughout the body and tail (see Table 1 for additional diagnostic features of the Amazonian triadal coralsnakes)
Redescription of the holotype ndash Head slightly distinct from body 367 mm SVL 33 mm TAL rostral vis-ible from above about twice as high as wide nasal semidivided rostral as high as long preocular single about twice as long as high postocular single about twice as high as long temporals 1+1 anterior tem-poral twice as long as high prefrontal length slightly longer than internasal supraocular twice as long as wide frontal twice as long as wide parietals about twice the width of frontal seven supralabials third and fourth contacting orbit seven infralabiais first four in contact with the anterior pair of chinshields anterior chinshields twice as long as wide posterior chinshields three times as long as wide cloacal plate divided three preventrals 295 ventral and 44 subcau-dal scales
Snout black including rostral first pair of su-pralabials and anterior portions of internasals pale (creamish white) band covering second pair of supra-labial posterior portions of nasals and prefrontals black band covering third to fifth supralabials pre and post-oculars anterior temporal supraocular frontal and anterior portion of parietals black cephalic band followed by red ring on the neck originates over the sixth supralabial posteriorly covering the seventh su-pralabial posterior temporal and posterior portion of parietals until the second dorsal Twenty one tri-ads along the body with 67 black 45 pale (creamish white) and 22 red rings including the post-cephalic stripe first body triad with large black ring dorsally 18th triad formed by five black and four pale rings
(= pentads) tail with one-mid triad with five black three pale and two red rings
Color pattern variation (Figures 2 and 3) ndash Snout with rostral first pair of supralabials anterior portions of nasal internasals and anterior portions of prefrontals generally uniformly black (Figure 2) an irregular pale band usually covers the posterior portions of second and anterior part of third pairs of supralabials pre-frontals and anterior portions of preoculars a large black band originates at posterior half of third pair of supralabials running to the anterior part of sixth pair of supralabials anterior temporal frontal and anterior portions of parietals parietal region with red ring limited by first body triad (Figures 3A B and C)Males having 11+frac12 to 23 and females 13 to 21+frac12 triads along the body middle black ring generally (four to six dorsal and three to five ventral scales in length) longer than the external black rings (generally three to four dorsal scales in length) pale rings (two to four dorsal or three to five scales in length) gener-ally with apical portion of each scale black tipped red rings (three to seven dorsal and three to eight ventral scales in length) generally with apical portion of each scale black tipped eventually triads might collapse forming pentads composed by five black and four to five pale rings (N = 4 including the holotype) gular region with symphysial cleft first four pairs of in-fralabials and first chin shields uniformly black (Fig-ure 3) belly scattered with small black dots on the red rings (Figure 2)
Meristic and morphometric variation (Table 2) ndash Third to fourth (N = 40) or third to fifth (N = 2) su-pralabials contacting orbit postoculars 01 (N = 1)11 (N = 14) 21 (N = 5) and 22 (N = 16) tempo-rals 1+1 (N = 35) and 1+2 (N = 1) generally four gu-lar scales (scales between last infralabials and chin shields) generally four preventrals ventrals 235-323(x = 2901 SD = 229 N = 23) in males and 231-323(x = 2924 SD = 321 N = 9) in females subcaudals 36-45 in males (Mean = 408 SD = 23 N = 23) and 32-41 in females (x = 382 SD = 23 N = 10 see Table 2 for additional variation on the meristic and morphometric characters)
Hemipenis (Figure 4) ndash Inverted organ (in situ)four subcaudals long bifurcating at second subcaudal level everted and maximally expanded organ short slightly bilobed and capitate sulcus spermaticus deep bifurcating on the terminal third of the hemipe-nial body with centrolineal orientation lobes short ornamented by few spines and spinules capitular
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
Feitosa DT et al 151
Diagnosis ndash Micrurus filiformis can be distinguished from all congeners by having the following com-bination of characters (1) slender body (diameter gt 5 mm) (2) black snout with a white band above internasals prefrontals and first two pairs of supral-abials (3) black band over most frontal and parietal shields (4) red gular scales (5) genials and first four pairs of infralabials uniformly black (6) 11-23 body triads (7) no supra-anal tubercles (8) ventral scales 270-316 in males and 275-333 in females (9) sub-caudal scales 33-45 in males and 30-41 in females (Figures 2 and 3)
Comparisons ndash Regarding all short-tailed Micruruswith the color pattern composed of triads (Slowinski 1995) M filiformis differs from them by having a very slender body (diameter gt 5 mm) and high num-ber of body triads (11-23)
With respect to the Amazon species of Micru-rus M filiformis is sympatric with at least eight taxa
of triadal coralsnakes It can be distinguished from M hemprichii hemprichii and M h ortoni by having a divided cloacal plate (vs single) 11-23 body triads (vs 7-10 in M h hemprichii and 5-6 in M h ortoni)and by the absence of a cephalic black cap (vs black cap originated in the rostral plate running to the post-
FIGURE 1 (A) Bivariate plot with 95 confidence regions for the first 2 axes derived from scores of PCA analysis for populations of Micrurus filiformis (B) Correlations of meristic characters with corresponding principal components (directional cosines) Num-ber of ventral scales = 1 and number of subcaudal scales = 2
FIGURE 3 Dorsal body view of Micrurus filiformis in life (MPEG21760) SVL 460 mm and TAL 35 mm Photograph by G Mas-chio
FIGURE 2 Dorsal (A) ventral (B) and lateral (C) views of Micru-rus filiformis (MPEG 21760) Scale = 5 mm
152 Taxonomic status of Micrurus filiformis
orbital region) from M surinamensis and M nattereriby having third and fourth supralabials contacting the orbit (vs fourth only) diameter of body lt 5 mm (vsbody diameter gt 5 mm) and by reaching a maximum total length of 700 mm (vs maximum total length 900 to 1350) from M spixii spixii M s martiusi and M s obscurus by the lack of a black cap (vs black cap from rostral to frontal plate) and by reaching a maximum total length of 700 mm (vs 1520 mm to 1600 mm maximum total length)
On the basis of general color pattern and hemipe-nial morphology Micrurus filiformis is traditionally placed in the Micrurus lemniscatus species group Re-garding the species currently comprising that group M filiformis is sympatric with M lemniscatus lem-niscatus M l diutius M l helleri and M isozonusbut differs from them by having a high number of ventrals subcaudals and triads throughout the body and tail (see Table 1 for additional diagnostic features of the Amazonian triadal coralsnakes)
Redescription of the holotype ndash Head slightly distinct from body 367 mm SVL 33 mm TAL rostral vis-ible from above about twice as high as wide nasal semidivided rostral as high as long preocular single about twice as long as high postocular single about twice as high as long temporals 1+1 anterior tem-poral twice as long as high prefrontal length slightly longer than internasal supraocular twice as long as wide frontal twice as long as wide parietals about twice the width of frontal seven supralabials third and fourth contacting orbit seven infralabiais first four in contact with the anterior pair of chinshields anterior chinshields twice as long as wide posterior chinshields three times as long as wide cloacal plate divided three preventrals 295 ventral and 44 subcau-dal scales
Snout black including rostral first pair of su-pralabials and anterior portions of internasals pale (creamish white) band covering second pair of supra-labial posterior portions of nasals and prefrontals black band covering third to fifth supralabials pre and post-oculars anterior temporal supraocular frontal and anterior portion of parietals black cephalic band followed by red ring on the neck originates over the sixth supralabial posteriorly covering the seventh su-pralabial posterior temporal and posterior portion of parietals until the second dorsal Twenty one tri-ads along the body with 67 black 45 pale (creamish white) and 22 red rings including the post-cephalic stripe first body triad with large black ring dorsally 18th triad formed by five black and four pale rings
(= pentads) tail with one-mid triad with five black three pale and two red rings
Color pattern variation (Figures 2 and 3) ndash Snout with rostral first pair of supralabials anterior portions of nasal internasals and anterior portions of prefrontals generally uniformly black (Figure 2) an irregular pale band usually covers the posterior portions of second and anterior part of third pairs of supralabials pre-frontals and anterior portions of preoculars a large black band originates at posterior half of third pair of supralabials running to the anterior part of sixth pair of supralabials anterior temporal frontal and anterior portions of parietals parietal region with red ring limited by first body triad (Figures 3A B and C)Males having 11+frac12 to 23 and females 13 to 21+frac12 triads along the body middle black ring generally (four to six dorsal and three to five ventral scales in length) longer than the external black rings (generally three to four dorsal scales in length) pale rings (two to four dorsal or three to five scales in length) gener-ally with apical portion of each scale black tipped red rings (three to seven dorsal and three to eight ventral scales in length) generally with apical portion of each scale black tipped eventually triads might collapse forming pentads composed by five black and four to five pale rings (N = 4 including the holotype) gular region with symphysial cleft first four pairs of in-fralabials and first chin shields uniformly black (Fig-ure 3) belly scattered with small black dots on the red rings (Figure 2)
Meristic and morphometric variation (Table 2) ndash Third to fourth (N = 40) or third to fifth (N = 2) su-pralabials contacting orbit postoculars 01 (N = 1)11 (N = 14) 21 (N = 5) and 22 (N = 16) tempo-rals 1+1 (N = 35) and 1+2 (N = 1) generally four gu-lar scales (scales between last infralabials and chin shields) generally four preventrals ventrals 235-323(x = 2901 SD = 229 N = 23) in males and 231-323(x = 2924 SD = 321 N = 9) in females subcaudals 36-45 in males (Mean = 408 SD = 23 N = 23) and 32-41 in females (x = 382 SD = 23 N = 10 see Table 2 for additional variation on the meristic and morphometric characters)
Hemipenis (Figure 4) ndash Inverted organ (in situ)four subcaudals long bifurcating at second subcaudal level everted and maximally expanded organ short slightly bilobed and capitate sulcus spermaticus deep bifurcating on the terminal third of the hemipe-nial body with centrolineal orientation lobes short ornamented by few spines and spinules capitular
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
152 Taxonomic status of Micrurus filiformis
orbital region) from M surinamensis and M nattereriby having third and fourth supralabials contacting the orbit (vs fourth only) diameter of body lt 5 mm (vsbody diameter gt 5 mm) and by reaching a maximum total length of 700 mm (vs maximum total length 900 to 1350) from M spixii spixii M s martiusi and M s obscurus by the lack of a black cap (vs black cap from rostral to frontal plate) and by reaching a maximum total length of 700 mm (vs 1520 mm to 1600 mm maximum total length)
On the basis of general color pattern and hemipe-nial morphology Micrurus filiformis is traditionally placed in the Micrurus lemniscatus species group Re-garding the species currently comprising that group M filiformis is sympatric with M lemniscatus lem-niscatus M l diutius M l helleri and M isozonusbut differs from them by having a high number of ventrals subcaudals and triads throughout the body and tail (see Table 1 for additional diagnostic features of the Amazonian triadal coralsnakes)
Redescription of the holotype ndash Head slightly distinct from body 367 mm SVL 33 mm TAL rostral vis-ible from above about twice as high as wide nasal semidivided rostral as high as long preocular single about twice as long as high postocular single about twice as high as long temporals 1+1 anterior tem-poral twice as long as high prefrontal length slightly longer than internasal supraocular twice as long as wide frontal twice as long as wide parietals about twice the width of frontal seven supralabials third and fourth contacting orbit seven infralabiais first four in contact with the anterior pair of chinshields anterior chinshields twice as long as wide posterior chinshields three times as long as wide cloacal plate divided three preventrals 295 ventral and 44 subcau-dal scales
Snout black including rostral first pair of su-pralabials and anterior portions of internasals pale (creamish white) band covering second pair of supra-labial posterior portions of nasals and prefrontals black band covering third to fifth supralabials pre and post-oculars anterior temporal supraocular frontal and anterior portion of parietals black cephalic band followed by red ring on the neck originates over the sixth supralabial posteriorly covering the seventh su-pralabial posterior temporal and posterior portion of parietals until the second dorsal Twenty one tri-ads along the body with 67 black 45 pale (creamish white) and 22 red rings including the post-cephalic stripe first body triad with large black ring dorsally 18th triad formed by five black and four pale rings
(= pentads) tail with one-mid triad with five black three pale and two red rings
Color pattern variation (Figures 2 and 3) ndash Snout with rostral first pair of supralabials anterior portions of nasal internasals and anterior portions of prefrontals generally uniformly black (Figure 2) an irregular pale band usually covers the posterior portions of second and anterior part of third pairs of supralabials pre-frontals and anterior portions of preoculars a large black band originates at posterior half of third pair of supralabials running to the anterior part of sixth pair of supralabials anterior temporal frontal and anterior portions of parietals parietal region with red ring limited by first body triad (Figures 3A B and C)Males having 11+frac12 to 23 and females 13 to 21+frac12 triads along the body middle black ring generally (four to six dorsal and three to five ventral scales in length) longer than the external black rings (generally three to four dorsal scales in length) pale rings (two to four dorsal or three to five scales in length) gener-ally with apical portion of each scale black tipped red rings (three to seven dorsal and three to eight ventral scales in length) generally with apical portion of each scale black tipped eventually triads might collapse forming pentads composed by five black and four to five pale rings (N = 4 including the holotype) gular region with symphysial cleft first four pairs of in-fralabials and first chin shields uniformly black (Fig-ure 3) belly scattered with small black dots on the red rings (Figure 2)
Meristic and morphometric variation (Table 2) ndash Third to fourth (N = 40) or third to fifth (N = 2) su-pralabials contacting orbit postoculars 01 (N = 1)11 (N = 14) 21 (N = 5) and 22 (N = 16) tempo-rals 1+1 (N = 35) and 1+2 (N = 1) generally four gu-lar scales (scales between last infralabials and chin shields) generally four preventrals ventrals 235-323(x = 2901 SD = 229 N = 23) in males and 231-323(x = 2924 SD = 321 N = 9) in females subcaudals 36-45 in males (Mean = 408 SD = 23 N = 23) and 32-41 in females (x = 382 SD = 23 N = 10 see Table 2 for additional variation on the meristic and morphometric characters)
Hemipenis (Figure 4) ndash Inverted organ (in situ)four subcaudals long bifurcating at second subcaudal level everted and maximally expanded organ short slightly bilobed and capitate sulcus spermaticus deep bifurcating on the terminal third of the hemipe-nial body with centrolineal orientation lobes short ornamented by few spines and spinules capitular
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
Feitosa DT et al 153
TABLE 1 Comaparisons of the meristics data between Micrurus filiformis and other Amazonian triad coralsnakes Data on variation except to M filiformis were extracted from Roze (1996) Campbell and Lamar (2004) and Passos and Fernandaes (2005)
Species Sex Ventrals Subcaudals Body triads Tail triadsM filiformis 270-316 33-45 1112 - 23 112 - 212
275-333 30-41 13-2112 112 - 212
M hemprichii hemprichii 156-193 20-34 7-10 1-113
160-191 22-28 7-9 1-113
M hemprichii ortoni 177-193 29-31 5-6 1178-185 21-26 5-6 1
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
154 Taxonomic status of Micrurus filiformis
sulcus evident in the sulcate side originating on the mid portion of hemipenial body running to the asul-cate side capitular sulcus becomes transversal on the asulcate side capitulum (about 60 of hemipenial body) ornamented by five to six irregular spine rows decreasing in size and number towards the apical por-tion of the lobes spines are irregular and very small on the asulcate side above the capitular groove ir-regular spines concentrated on the sulcate side the base of the organ is nude basal pocket located on the sulcate side and delimited by a central protuberance ornamented by few spinules internal portion of basal pocket with few irregular spinules
Distribution (Figure 5) ndash Widely distributed in the Upper Amazon Basin from Colombia to Peru in the eastern versant of the Andes and Brazilian Amazoniaoccurring in primary and secondary forests riparian forests and eventually in open forests and Neotropi-cal savannas Additional records for the species were compiled from Campbell and Lamar (2004)
DISCUSSION
Roze (1967) described Micrurus filiformis subtilisbased on four specimens from the ColombiaBrazilborder differing from the nominal race by having two postoculars and 274-279 ventral scales in males (vssingle postocular and 283-309 in females of M f fi-liformis) Nevertheless Dixon and Soini (1977) and Cunha and Nascimento (1978 1982) whilst compar-ing samples recognized as M f filiformis from Peruand Brazil respectively found considerable varia-
tion in the number of ventral and postocular scales Roze (1996) provided a comprehensive revision of the genus in which he accepted the synonymyzation of both subspecies as suggested earlier by Cunha and Nascimento (1978) Since the range of ventral scales in M f subtilis largely extends the known variation of M f filiformis the meristic morphometric and color pattern variation reported in our study corrobo-rates this assertion Moreover all statistical tests per-formed were unable to discriminate both subspecies Although the principal components analysis reveled some discrimination between groups in the second axis (Figure 1A) this factor was strongly correlated with the number of subcaudal scales (Figure 1B)Owing to the small sample size of females we could not find any clear sexual dimorphism in this species based on subcaudal scales even knowing that this is a peculiar widespread characteristic in snakes (Ta-ble 1)
Coralsnakes of the genus Micrurus comprising two mainly monophyletic lineages are recognized primarily by their color pattern formed by monads or triads and relative tail sizes (see Slowinski 1995) These lineages also shared diagnostic characters based on hemipenial morphology (Slowinski 1995 Roze 1996) Micrurus filiformis has a short and slightly bilobed hemipenis a characteristic shared by most of the triadal species of Micrurus occurring in Amazonia (M l lemniscatus M l diutius M l hel-leri M h hemprichii M spixii spixii M spixii mar-tiusi and M spixii obscurus) Nonetheless compared to the above assemblage M filiformis shows a very slender body (diameter lt 5 mm) higher number of body triads (11-23) a short hemipenis (inverted or-gan is four subcaudals long) with spines concentrated mostly on the hemipenial body
The statistical tests performed were unable to find significant differences in SVL number of ventral scales and number of body triads between males and females of Micrurus filiformis Usually species that do not show sexual dimorphism in SVL andor num-ber of ventral scales are interpreted as taxa having male-male combat (Shine 1978 Madsen and Shine 1993 Shine 1994) This kind of behavior is uncom-mon in the genus Micrurus having been previously documented the Neotropics only for the southern South American species M altirostris (Almeida-San-tos et al 1998) Since the genus includes mainly two monophyletic lineages and this behavior was never been reported for the monadal clade we suggest that it can be expected to occur in M filiformis and other triadal species
FIGURE 4 Sulcate (A) and asulcate (B) sides of the hemipenis of Micrurus filiformis (rigth organ MPEG 20948) Scale = 5 mm
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
Feitosa DT et al 155
RESUMO
O posicionamento taxonocircmico de Micrurus filifor-mis eacute reavaliado empregando-se meacutetodos estatiacutesticos Micrurus filiformis subtilis eacute mantida na sinoniacutemia de M filiformis baseado nos resultados de anaacutelises quantitativas e qualitativas Adicionalmente satildeo des-critas variaccedilotildees geograacuteficas dos caracteres meriacutesticos morfomeacutetricos e hemipecircnis O holoacutetipo de Micrurusfiliformis eacute redescrito
ACKNOWLEDGEMENTS
We are grateful to the following curators for permission andor for facilitating the examination of specimens under their care F Franco (IBSP) R Casallas and A Rodriguez (MLS) J Lynch (ICN) and R Vogt (INPA) We thank Gleomar Maschiofor permission to use their photographs J Mueses-Cisneros for help in the ICN collection C McCarthy (NHM) for providing data and photographs of the holotype of Micrurus filiformis We thank W Wosiack (MPEG) for suggestions that have improved the manuscript D T Feitosa and P Passos thank the Conselho
Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq)and Coordenaccedilatildeo de Aperfeiccediloamento de Pessoal de Niacutevel Su-perior (CAPES) for financial support A L C Prudente thanks Conselho Nacional de Desenvolvimento Cientiacutefico e Tecnoloacutegico (CNPq grant no 4760962006-5)
LITERATURE CITED
ALMEIDA-SANTOS S M L F S AGUIAR AND R L BALESTRIN1998 Micrurus frontalis (Coral Snake) Male combat Her-petological Review 29242
AMARAL A 1925 South American Snakes in the collection of the United States National Museum Proceedings of UnitedStates Natural Museum 671-30
BOULENGER G A 1896 Catalogue of the Snakes in the British Museum of the Natural History Vol 3 Trusties of the British Museum London 727 pp
CAMPBELL J A AND W W LAMAR 1989 The venomous reptiles of Latin America Ithaca Comstock Publishing AssociatesCornell University Press Ithaca New York USA 425 pp
CAMPBELL J A AND W W LAMAR 2004 The venomous reptiles of western hemisphere Vol 1 Comstock Publishing Associates Cornell University Press Ithaca New York USA 476 pp
FIGURE 5 Geographic distribution of Micrurus filiformis Specimens examined are represented by a dot Literature records were extracted
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
PARAacute Acaraacute Boa Vista (MPEG 21491 right or-gan) Melgaccedilo Estaccedilatildeo Cientiacutefica Ferreira Penna(MPEG 20948 left organ)
156 Taxonomic status of Micrurus filiformis
CUNHA O R AND F P NASCIMENTO 1978 Ofiacutedios da AmazocircniaX As cobras da Regiatildeo Leste do Paraacute Publicaccedilotildees Avulsasdo Museu Paraense Emiacutelio Goeldi 31156-170
CUNHA O R AND F P NASCIMENTO 1982 Ofiacutedios da Amazocircnia XIV As espeacutecies de Micrurus Bothrops Lachesis e Crota-lus do Sul do Paraacute e Oeste do Maranhatildeo incluindo aacutereas de cerrado deste estado (Ophidia Elapidae Viperidae) Boletim Museu Paraense Emiacutelio Goeldi Seacuterie Zoologia 1121-58
CUNHA O R AND F P NASCIMENTO 1993 Ofiacutedios da AmazocircniaAs cobras da Regiatildeo Leste do Paraacute Boletim do Museu Par-aense Emiacutelio Goeldi Seacuterie Zoologia 91-191
DIXON J R AND P SOINI 1977 The Reptiles of the upper Ama-zon Basin Iquitos region Peru II ndash Crocodilians turtles and snakes Contributions in Biology and Geology MilwaukeePublic Museum Monograph 121-91
DOWLING H G 1951 A proposed standard system of counting ventrals in snakes Journal of Herpetology 197-99
GOMES J F 1918 Contribuiccedilatildeo ao conhecimento dos ofiacutedios do Brasil III 1 Ophidios do Museu Paraense Memoacuterias do In-stituto Butantan 157-83
GUumlNTHER G A 1859 On the Genus Elaps of Wagler Proceed-ings of the Zoological Society of London 2779-89
LEVITON A E R H GIBAS JR E HEAL AND C E DAWSON 1985Standards in Herpetology and Ichthyology Part 1 Standard codes for institutional resource collection in herpetology and ichthyology Copeia 1985802-832
MADSEN T AND R SHINE 1993 Temporal variability in sexual selection acting on reproductive tactics and body size in male snakes The American Naturalist 141167-171
MANLY B F J 2000 Multivariate statistical methods A primer 2nd ed Chapman and Hall Press New York USA 215 pp
MANZANI P R AND A S ABE 1988 Sobre dois novos meacutetodos de preparo de hemipecircnis de serpentes Memoacuterias do InstitutoButantan 5015-20
MATHWORKS 1994 Matlab for windows version 42c1 NatickThe MathWorks Inc Texas Tech University USA
PASSOS P AND D S FERNANDES 2005 Variation and taxonomic status of the aquatic coral snake Micrurus surinamensis (Cu-vier 1817) (Serpentes Elapidae) Zootaxa 9531-14
PASSOS P R FERNANDES AND M PORTO 2005 Geographical variation and taxonomy of the Snail-eating snake Dipsas al-bifrons (Sauvage 1884) with comments on the systematic status of Dipsas albifrons cavalheiroi Hoge 1950 (Serpentes Colubridae Dipsadinae) Zootaxa 101319-34
PEacuteREZ-SANTOS C AND A G MORENO 1988 Ofiacutedios da ColocircmbiaMuseu Regionale de Scienze Natural Torino Monographie43661-402
PESANTES O 1994 A method for preparing the hemipenis of pre-served snakes Journal of Herpetology 2893-95
ROZE J A 1967 A Check list of the New World Venomous coral snakes (Elapidae) with description of new forms AmericanMuseum Novitates 22871-70
ROZE J A 1982 New World Coral Snakes (Elapidae) a taxo-nomic and biological summary Memoacuterias do Instituto Bu-tantan 46305-338
ROZE J A 1996 Coral Snakes of the Americas Biology Identi-fication and Venoms Krieger Publishing Company MalabarFlorida USA 328 pp
SAVAGE J M AND J B SLOWINSKY 1992 The colouration of the venomous coral snakes (Family Elapidae) and their mimics (families Aniliidae and Colubridae) Biological Journal of the Linnean Society 45235-254
SHINE R 1978 Sexual size dimorphism and male combat in snakes Oecologia 33269-277
SHINE R 1994 Sexual size dimorphism in snakes revisited Co-peia 1994326-346
SLOWINSKI J B 1995 A Phylogenetic analysis of the New world Coral Snakes (Elapidae Leptomicrurus Micruroides and Micrurus) Based on allozymic and morphological characters Journal of Herpetology 29325-338
STATSOFT 2003 Statistica for Windows version 60 Tulsa Stat-soft Inc USA
STRAUSS R E 1985 Evolutionary allometry and variation in body form in the South American catfish genus Corydoras(Callichthyidae) Systematic Zoology 34381-396
WIENS J J AND M SERVEDIO 2000 Species delimitation in sys-tematics inferring diagnostic differences between species Proceedings of the Royal Society of London Biological Sci-ences 267631-636
ZAHER H AND A L C PRUDENTE 1999 Intraespecific variation of the hemipenis in Siphlophis and Tripanurgos Journal of Herpetology 33702-706
ZAHER H AND A L C PRUDENTE 2003 Hemipenis of Siphlo-phis (Serpentes Xenodontinae) and techniques of hemipenial preparation in snakes A response to Dowling Herpetological Review 34302-307
ZAR J H 1999 Bioestatistical analysis 4th ed Prentice-HallPress New Jersey USA 633 pp
