A new species of Microcaecilia (Amphibia: Gymnophiona: Siphonopidae) from the Guianan region of Brazil

Zootaxa 3693 (3): 387–394 www.mapress.com /zootaxa / ISSN 1175-5326 (print edition) Article Copyright © 2013 Magnolia Press ZOOTAXA ISSN 1175-5334 (online edition) https://dx.doi.org/10.11646/zootaxa.3693.3.9 https://zoobank.org/urn:lsid:zoobank.org:pub:E579E038-15E1-465E-9CA0-08F5758E1E3A A new species of Microcaecilia (Amphibia: Gymnophiona: Siphonopidae) from the Guianan region of Brazil ADRIANO O. MACIEL1, 2 & MARINUS S. HOOGMOED1 ¹Museu Paraense Emílio Goeldi, Coordenação de Zoologia, 66077-530 Belém, Pará, Brazil Corresponding author. E-mail: [email protected] 2 Abstract We describe a new species of Microcaecilia from the Guianan region of Brazil, based on a series of eight specimens from the states of Pará and Amazonas. Microcaecilia marvaleewakeae sp. nov. is very similar to M. taylori, but differs from it in having more primary annuli, more secondary grooves, and more secondary grooves that completely encircle the body. The new species also seems to have a relatively shorter and thinner head than M. taylori, but additional specimens of the new species are necessary to check this. A brief discussion of the taxonomy of M. taylori is presented. Key words: Amazonia, caecilians, herpetology, Microcaecilia taylori, taxonomy Resumo Nós descrevemos uma nova espécie de Microcaecilia da região das Guianas, do Brasil com base em uma série de oito espécimes. Microcaecilia marvaleewakeae sp. nov. é muito semelhante a M. taylori, mas difere desta por ter mais anéis primários, mais ranhuras secundárias e mais ranhuras secundárias que circundam completamente o corpo. A nova espécie também aparenta ter uma cabeça relativamente menor e mais fina que M. taylori, mas espécimes adicionais da nova espécie são necessários para verificar isso. Uma breve discussão sobre a taxonomia de M. taylori é apresentada. Palavras-chave: Amazônia, cecílias, herpetologia, Microcaecilia taylori, taxonomia Introduction Among caecilian amphibians (Gymnophiona) of the Siphonopidae Bonaparte, 1850, recently resurrected by Wilkinson et al. (2011), Microcaecilia Taylor, 1968 is the most speciose genus of the family, including 12 species, most from the Guianan region of South America (Maciel & Hoogmoed, 2011a; Wilkinson et al. 2013; Donnelly & Wake, 2013). Currently four species of the genus are known in Brazil, three of them from few localities in Amazonia (Maciel & Hoogmoed, 2011a). While examining some Microcaecilia from the Brazilian states of Amazonas and Pará, we found specimens very similar to M. taylori Nussbaum & Hoogmoed, 1979, but which differ from the latter in numbers and completeness of annular grooves, and in morphometric characters. We here describe this material as a new species. Material and methods All measurements were taken using a dial caliper to the nearest 0.1 mm, except total length, which was taken with a ruler to the nearest 1 mm. We examined specimens from four herpetological collections (Appendix 1): MNRJ, Museu Nacional, Rio de Janeiro, Brazil; MPEG, Museu Paraense Emílio Goeldi, Belém, Pará, Brazil; IEPA, Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá; RMNH, Rijksmuseum van Natuurlijke Accepted by David Gower: 13 Jul. 2013; published: 30 Jul. 2013 387 Historie, Leiden, The Netherlands. The sex and maturity of all specimens were determined by direct observation of the gonads. Searching for dermal and subdermal scales was made at 80x magnification under a stereo microscope. Maciel & Hoogmoed (2011a, b) used “terminal shield” to describe the posteriormost segment of many species, including those of Microcaecilia. Here we use “terminal cap” for the small terminal segment that is posterior to the vent in Microcaecilia, as suggested by Kotharambath et al. (2012). All measurements and counts were taken by the first author. In the morphological comparisons we only used the morphometric data from one of the type specimens of M. taylori (RMNH 15165B), to which we have access. Some of our data for RMNH 15165B differ from those reported by Nussbaum & Hoogmoed (1997) for this paratype. The measurement of the choanae was possible in five paratypes, for which we recorded the greatest width of the right choana and the distance between the choanae. Microcaecilia marvaleewakeae sp. nov. (Figs. 1–4; Tables 1–2) Holotype. MPEG 21896, mature female (Fig. 1), from Platô Bacaba (S 1° 46’ 23’’, W 56° 22’ 14’’, elevation 76 m), Flona Saracá-Taquera, municipality of Oriximiná, State of Pará, Brazil, 8-VI-2007, collected by G. F. Maschio. Paratypes. 6 specimens. MPEG 20655, mature male, from Platô Bela Cruz (S 1° 48’ 1’’, W 56° 30’ 20’’, 160 m), Flona Saracá-Taquera, municipality of Oriximiná, State of Pará, Brazil, 24-XII-2006, collected by E. G. Pereira; MPEG 26946, mature male, from municipality of Urucará, State of Amazonas, Brazil, 11:13 am, 6-II2009, collected by E. G. Pereira using general herpetological search methods in a forested area; MPEG 28117, mature female, from municipality of Urucará (S 2° 24’ 9’’, W 57° 37’ 45’’, 50 m), State of Amazonas, Brazil, 6-X2009, collected by H. Kuffner using general herpetological search methods in a forested area; MNRJ 47878, mature female, from Flona Saracá-Taquera (S 1° 48’ 1’’, W 56° 30’ 20’’, 160 m), municipality of Oriximiná, State of Pará, Brazil, 29-XII-2006, collected by E. G. Pereira. MNRJ 56700, mature female (Fig. 2), from municipality of Urucará (S 2° 23’ 50’’, W 57° 37’ 45’’, 90 m), State of Amazonas, Brazil, 11:44 am, 2-II-2009, collected by E. G. Pereira, R. A. K. Ribeiro, R. W. Ávila & J. A. Scalzo using general herpetological search methods in a forested area. MNRJ 64012 male, from Marajatuba, municipality of Urucará, State of Amazonas, Brazil, 5-X-2009, collected by R. W. Ávila. Referred specimen. MNRJ 872, from Serra do Ererê (approximately S 1° 52’, W 54° 11’, 65 m), municipality of Monte Alegre, State of Pará, Brazil with no more data. Excluded from the type series because it was very desiccated and we could not record most measures, or determine the sex. Diagnosis. The new species is a Microcaecilia because it has the eye under bone, tentacle aperture closer to eye than to naris, and no diastema between vomerine and palatine teeth. Microcaecilia marvaleewakeae has a known range of 124–138 primary annuli, 21–33 secondary grooves, premaxillary-maxillary teeth extend behind posterior margin of choanae; vomeropalatine teeth bicuspid; dermal scales present; no indication of subdermal scales. Microcaecilia marvaleewakeae differs from M. albiceps (Boulenger, 1882), M. grandis Wilkinson, Nussbaum & Hoogmoed, 2009, M. rabei (Roze & Solano, 1963), M. savagei Donnelly & Wake, 2013, M. trombetas Maciel & Hoogmoed, 2011, M. unicolor (Duméril, 1863), M. iyob Wilkinson & Kok, 2010, and M. dermatophaga Wilkinson, Sherratt, Starace & Gower, 2013 in having more primary grooves (more than 123). Distinct from M. dermatophaga also in having more secondary grooves (more than 9), and a greater maximum number of complete secondary grooves (more than 3). From M. supernumeraria Taylor, 1969 it differs in having fewer primary (less than 143) and secondary grooves (less than 93). Distinct from M. grandis and M. rochai Maciel & Hoogmoed, 2011 in having fewer secondary grooves (less than 42). Distinct from M. albiceps, M. savagei, M. supernumeraria, M. trombetas, and M. unicolor in having bicuspid instead of monocuspid vomeropalatine teeth. Microcaecilia marvaleewakeae differs slightly from M. taylori in having a greater maximum number of primary grooves (138 versus 130), and the new species has more secondary grooves (more than 20; Table 1, 2), and a greater maximum number of complete secondary grooves (more than 6; Table 1, 2). Description of the holotype. Adult female (Fig. 1), total length 158 mm. Multiple small oocytes, abundant fat bodies. Longitudinal ventral incision approximately 10 mm long near end of body (89th to 98th primary annulus). Total length 41.6 times body width. Head slightly narrower than body; dorsum of head slightly convex in lateral 388 · Zootaxa 3693 (3) © 2013 Magnolia Press MACIEL & HOOGMOED view. Margin of upper jaw straight in lateral view, no concavity formed at level of tentacular openings. Snout projects 1 mm beyond mouth. Tip of snout rounded. Nostrils subcircular, visible from above. Eyes not visible. Tentacular openings circular, slightly elevated above skin, laterally positioned, near margin of mouth, slightly closer to corner of mouth than to nostrils, visible from above. TABLE 1. Comparisons between Microcaecilia marvaleewakeae sp. nov. and M. taylori showing ranges, means and standard deviations, with numbers of specimens given in parentheses. M. marvaleewakeae M. taylori Males (3) Females (4) Males (46) Females (54) Head length / head width 1.3–1.6 1.4 ± 0.1 1.4–1.5 1.42 ± 0.04 1.2–1.6 1.4 ± 0.1 1.2–1.7 1.4 ± 0.1 Total length / head length 32.1–41.7 37.6 ± 4.9 34.7–39.5 37.6 ± 2.1 22–37.5 31.1 ± 3.3 26.8–40 32.7 ± 2.7 Total length / head width 51.9–59.1 54.6 ± 3.9 48.6–58.5 53.8 ± 4 33.9–55 44.4 ± 4.3 39.9–54 46.7 ± 3.2 Both sexes Both sexes Primary annuli 124–138 130.4 ± 4 (8) 113–130 123.2 ± 3.2 (108) Secondary grooves 21–33 25 ± 4 (8) 0–21 2.2 ± 4.5 (108) Complete secondaries 4–8 6.1 ± 1.6 (7) 0–6 0.2 ± 1 (108) FIGURE 1. Holotype of Microcaecilia marvaleewakeae sp. nov. (MPEG 21896). Left column: head and anterior part of body dorsally (above), laterally (middle) and ventrally (below). Right column: posterior part of body dorsally (above), laterally (middle) and ventrally (below). A NEW SPECIES OF MICROCAECILIA FROM BRAZIL Zootaxa 3693 (3) © 2013 Magnolia Press · 389 390 · Zootaxa 3693 (3) © 2013 Magnolia Press MACIEL & HOOGMOED FIGURE 2. A paratype of Microcaecilia marvaleewakeae sp. nov. (MNRJ 56700) in life. Head and anterior part of body (left) and general view (right). Photos: R. A. K. Ribeiro. FIGURE 3. Map of distribution of Microcaecilia marvaleewakeae sp. nov. (circles) and M. taylori (triangles). 1. Type locality of M. taylori, Sipaliwini, Suriname, 2. Urucará, Amazonas, Brazil, 3. Type locality of M. Marvaleewakae sp. nov., Oriximiná, Pará, Brazil, 4. Serra do Ererê, Monte Alegre, Pará, Brazil. A NEW SPECIES OF MICROCAECILIA FROM BRAZIL Zootaxa 3693 (3) © 2013 Magnolia Press · 391 Nuchal grooves distinct dorsally, laterally and ventrally, completely encircling body. First collar (1.1 mm) shorter than second (1.6 mm). Single dorsal transverse groove present on each collar, approximately same size. Body subcylindrical, slightly wider than deep. Width along body varies slightly, narrower at terminal region. Primary annuli 129. Primary annular grooves completely encircling the body, except two that are interrupted by the vent. Small terminal cap present posterior to vent. Secondary grooves 27; seven secondary grooves complete. One secondary annular groove posterior to level of posterior margin of vent. Vertical “keel” present on tip of body terminus. Vent with 13 denticulations: seven anterior, six posterior. Dermal scales starting at 45th annular groove, with at most 4 rows per annulus. Scales at 45th primary groove small, narrow, (0.1 x 0.2 mm); larger posteriorly (e.g. 0.3 x 0.5 mm at 100th primary groove). Choanae circular, due to the partially closed mouth it was not possible to measure them. Tongue anteriorly attached to mandibular mucosa, without narial plugs. Lower jaw broken anteriorly. Mouth slightly opened, premaxillary-maxillary and dentary teeth visible externally. Premaxillary-maxillary teeth 20, little variation in size, posterior maxillary teeth smaller. Premaxillary-maxillary series extending behind level of choanae. Vomeropalatine teeth 22, bicuspid, with no apparent variation in size; teeth smaller than in all other series. Dentary teeth 15, slightly larger than premaxillary-maxillary teeth; size of teeth decreasing posteriorly. Also see Table 2. Colour. In life (based on photographs of MNRJ 56700 made in the field by R. A. K. Ribeiro; Fig. 2): body dark lavender, gradually paler towards pinkish head. Venter and lateral surface slightly paler than dorsum along entire body. Area surrounding vent less pigmented, as are mandible and part of head. Annular grooves on sides of body slightly paler than general body colour. In preservative grayish or brownish with lateral and ventral surfaces of body slightly paler than dorsum. Annular grooves on sides of body slightly darker than general body colour. Variation. There is little variation among the type specimens (Table 2). Two specimens (MNRJ 56700 and 64012) lack a dorsal transverse groove on the first collar. The referred specimen from the easternmost known locality (MNRJ 872) has five more primary annuli than the types and one of the lowest counts of secondary grooves, but it is too poorly preserved to make more detailed comparisons of many features. FIGURE 4. Two adult females: above, holotype of Microcaecilia marvaleewakeae sp. nov. (MPEG 21896; total length 158 mm; head width 2.7 mm; head length 4 mm); below, specimen of M. taylori (MPEG 22129 from south of the Amazon; total length 143 mm; head width 3.3 mm; head length 5.1 mm). 392 · Zootaxa 3693 (3) © 2013 Magnolia Press MACIEL & HOOGMOED Distribution. Only known from the localities where holo- and paratypes were collected in the States of Amazonas, and Pará, Brazil. (Fig. 3). Etymology. It is with great pleasure that we name this species in honor of Dr. Marvalee H. Wake, professor of the Department of Integrative Biology, University of California, Berkeley, USA; one of the most important present day researchers of caecilians and author of many publications on development, morphology, phylogeny, and reproductive biology of these secretive animals. Remarks. Microcaecilia marvaleewakeae apparently differs from M. taylori in having a more slender and smaller head (Fig. 4). For example, a paratype of M. taylori (RMNH 15165B; male, total length 122 mm; head width 3.3 mm; head length 4.5 mm) has a wider head than male paratypes of M. marvaleewakeae with greater total lengths (e.g. MPEG 20655, total length 164 mm; head width 3.1 mm; head length 4.2 mm, and MPEG 26946, total length 135 mm; head width 2.6 mm; head length 4.2 mm). However, in comparisons of ratios of head measures and body size we find no clear differences between the species (Table 1), only total length:head width seems to be different, but more specimens are necessary to solve this question. Wilkinson et al. (2013) described M. dermatophaga based on nine specimens from French Guiana, very similar to M. taylori but reportedly differing from it in lacking a transverse groove on the first collar. Re-examining the specimens of M. taylori documented by Maciel & Hoogmoed (2011b) and additional recently collected specimens, we found that we previously overlooked that some individuals have no transverse groove on the first collar (27 of 161 analyzed specimens; 16.7% of the sample). However, M. dermatophaga remains distinct from M. taylori (sensu Maciel & Hoogmoed, 2011b) because it generally has fewer primary grooves (107–113 [n = 9] vs. 113–130 [n = 125]), and a higher mean number of secondary grooves (7.2 [n = 9] vs. 2.2 [n = 123]). Discussion Resolving the taxonomy of Microcaecilia (now 12 nominal species) is challenging given the recent increase in described species and still generally small sample sizes and few diagnostic characters (see also Wilkinson et al., 2013; Donnelly & Wake, 2013). The approximately 680 km gap in the distribution of M. taylori (Fig. 3) is intriguing and opens the question of whether the specimens from south of the Amazon River are not M. taylori (see also Wilkinson et al., 2013) or whether this disjunction is instead a sampling gap reflecting the difficulty of finding caecilians during traditional herpetofaunal inventories (Maciel & Hoogmoed, 2011b). Maciel & Hoogmoed (2011b) analyzed 128 M. taylori-like specimens from south of the Amazon, and found that the range in meristic (annuli and teeth number) and morphometric data, as well as tooth series length, tooth cusps and size at which sexual maturity is reached, exceeds and encompasses the range of the Suriname type specimens. Microcaecilia taylori was described on the basis of three specimens lacking secondary grooves, the first known species of Microcaecilia with this condition (Nussbaum & Hoogmoed, 1979). In 86 of 125 (68%) Brazilian specimens analyzed by Maciel & Hoogmoed (2011b), the secondary grooves are absent, as in the three type specimens. Additionally, the variation in this character is geographically widespread, with each of the studied populations (Fig. 3) having some specimens with few incomplete secondary grooves (Maciel & Hoogmoed, 2011b). The variation in this character (absence or presence of secondary grooves) was previously reported for species of other siphonopids, for example, Brasilotyphlus guarantanus Maciel, Mott & Hoogmoed 2009, apparently closely related to Microcaecilia, which may have or lack secondary grooves; three of the 48 types have two incomplete secondary grooves (Maciel et al., 2009). A clear resolution of the taxonomy of M. taylori possibly will need the study of new characters, and new collections in or near the type locality to obtain tissue samples for molecular evaluation. Acknowledgments We thank Ana L. Prudente and Fabrício Sarmento (MPEG), Jucivaldo Lima (IEPA), Ronald de Ruiter (RMNH), José Pombal Junior and Pedro Pinna (MNRJ) for the loan of specimens, and Ricardo Kawashita Ribeiro for providing the picture of a live specimen. David Gower, Mark Wilkinson, and an anonymous referee provided helpful suggestions on the submitted manuscript. The first author is supported financially by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES). A NEW SPECIES OF MICROCAECILIA FROM BRAZIL Zootaxa 3693 (3) © 2013 Magnolia Press · 393 References Donnelly, M.A. & Wake, M.H. (2013) A new Microcaecilia (Amphibia: Gymnophiona) from Guyana with comments on Epicrionops niger. Copeia, 2013, 223–231. Duméril, A.M.C. (1863) Catalogue Méthodique de la collection des batraciens du Múseum d’histoire naturelle de Paris. Mémoirs de la Société Impériale des Sciences Naturelles Cherbourg. Kotharambath, R., Gower, D.J., Oommen, O.V. & Wilkinson, M. 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(2013) A new species of skin-feeding caecilian and the first report of reproductive mode in Microcaecilia (Amphibia: Gymnophiona: Siphonopidae). PLoS One, 8(3), e57756. https://dx.doi.org/10.1371/journal.pone.0057756 APPENDIX 1 Specimens analyzed (number of specimens of each species in parenthesis), excluding types of Microcaecilia marvaleewakeae sp. nov. (listed in main text). Microcaecilia rochai (4) BRAZIL: PARÁ: Almeirim (MPEG14596–14597); AMAPÁ: Laranjal do Jari (IEPA/TQ 233), Pracuúba (IEPA/TQ 721). Microcaecilia taylori (175) SURINAME: SIPALIWINI: (RMNH 15165B) BRAZIL: PARÁ: Curionópolis (MPEG 35719), Marabá (MPEG 29092–29095), Melgaço (MPEG 5746–5748, 6660, 6670, 23360–23366, 26947, 35714, 35715, RMNH 40187), Pacajá (MPEG 35505), Parauapebas (MPEG/PSH007, 014; MPEG 7350–7353, 16230, 22074–22169, 22171, 22172), Portel (MPEG 22779–22783), Rondon do Pará (MPEG 32560), Santarém (MPEG 743), Tucuruí (MPEG 3761), Vitória do Xingu (MPEG 10106; MPEG/Xingu 86, 279, 291–296, 311, 312, 324, 325, 327, 339, 340, 346, 347, 420, 421, 434, 483, 552, 561, 562, 593, 594, 597, 598, 601–603, 618, 625, 650–654), Xinguara (MNRJ 55707). Microcaecilia trombetas (1) BRAZIL: PARÁ: Óbidos (MPEG 26476). 394 · Zootaxa 3693 (3) © 2013 Magnolia Press MACIEL & HOOGMOED