First georeferenced record of Amphisbaena fuliginosa Linnaeus, 1758 for the State of Ceará, northeastern Brazil (Squamata, Amphisbaenidae)
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Herpetology Notes, volume 14: 639-643 (2021) (published online on 10 April 2021) First georeferenced record of Amphisbaena fuliginosa Linnaeus, 1758 for the State of Ceará, northeastern Brazil (Squamata, Amphisbaenidae) Igor Joventino Roberto1,*, João Rafael Muniz Silva2, Thieres Pinto3, and Robson Waldemar Ávila1 Amphisbaena fuliginosa Linnaeus, 1758 is a large- by a colouration pattern fitting A. f. wiedi. However, sized stout-bodied amphisbaenian, characterised by there were no specific localities associated with these a maximum total length of 500 mm, 6–10 precloacal specimens. Vanzolini (2002) included additional pores, 190–220 body annuli, 23–30 tail annuli, and a specimens from the Cerrado biome of Central Brazil, brindled colour pattern varying between a yellowish but did not include the individuals from Ceará. In this to purplish background and with different degrees of paper, the author mentioned that A. f. wiedi had a wider dark spots (Vanzolini, 1951, 2002). This species has a distribution south of the Amazon River. Ribeiro et al. wide geographic distribution from Panamá throughout (2012) provided a record of A. fuliginosa from the the Amazon, with disconnected populations in the Chapada do Araripe, southern Ceará, and mentioned Cerrado biome in Central Brazil, the Atlantic Forest in a specimen from the São Paulo collection (MZUSP northeastern Brazil, and an isolated population in the 7059), but this specimen is only listed with Ceará State state of Ceará, in the Caatinga biome (Vanzolini, 2002; as a general locality (Roberto and Loebmann, 2016). Costa and Bérnils, 2018). Costa and Bérnils (2018) tentatively assigned the Amphisbaena fuligionosa is considered a polytypic populations of central and northeastern Brazil to A. f. species, composed of five subspecies, including A. f. wiedi, including the populations in Ceará State, based fuliginosa Linnaeus, 1758, A. f. amazonica Vanzolini, on geographic distribution. Nevertheless, it appears that 1951, A. f. bassleri Vanzolini, 1951, A. f. varia Laurenti, so far, no specific geographic locality is associated with 1768, and A. f. wiedi Vanzolini, 1951 (Vanzolini, Ceará populations of A. fuliginosa. We here provide 1951, 2002). However, morphological characters such a record. overlap significantly between these taxa, making their identification difficult. During his taxonomic review of A. fuliginosa, Vanzolini (1951) included three specimens from Ceará State. Two of these had 214 body annuli, 24–25 tail annuli, 8–10 pores, and 22/24 to 24/24 segments at the midbody annulus, fitting in the range of variation for A. f. amazonica, whereas the third individual had 203 body annuli, 27 tail annuli, and 20/20 segments at the midbody annulus, accompanied 1 Departamento de Biologia, Universidade Federal do Ceará, Avenida. Mister Hull s/n, Pici, Fortaleza, Ceará 60455-760, Brazil. 2 Instituto Centro de Ensino Tecnológico, Rua Silva Jardim 515, José Bonifacio, Fortaleza, Ceará 60040-260, Brazil. 3 Sertões Consultoria Ambiental e Assessoria, Avenida Oliveira Figure 1. Individual of Amphisbaena fuliginosa, photographed Paiva 2797, Fortaleza, Ceará 60821-740, Brazil. while crossing a dirt road at São Felix, Viçosa do Ceará * Corresponding author. E-mail: igorjoventino@yahoo.com.br Municipality, Ceará State, northeastern Brazil. Photo by João © 2021 by Herpetology Notes. Open Access by CC BY-NC-ND 4.0. Rafael Muniz Silva.
640 Igor Joventino Roberto et al. On 11 February 2019 at 08:08 h, JRMS observed an more mottled colour pattern (see Figs. 1–4 in Vanzolini, individual of A. fuliginosa (Fig. 1) crossing a dirt road 2002; Lemos and Facure, 2007; Nogueira-Costa et al., at São Felix, Viçosa do Ceará Municipality, Ceará State, 2013) than the Santa Maria and this Ceará population. Brazil (3.428°S, 41.184°W). This locality is within the Based on the colouration pattern and the distribution boundaries of the Área de Proteção Ambiental Serra (see Table 1, Fig. 2), we consider this record in Ceará as da Ibiapaba (APA – Environmental Protection Area A. fuliginosa wiedi. However, a taxonomic assessment of Ibiapaba Mountain Range). The vegetation of the of A. fuliginosa is still needed to verify the validity of area is a transition between humid forest and degraded the subspecies within this species complex (Costa and arboreal Caatinga, with a dark red latosol (Loebmann Bérnils, 2018). and Haddad, 2010). The Planalto da Ibiapaba harbours several reptile We were, unfortunately, unable to collect the individual and amphibian taxa with Amazon origin (Roberto to access meristic data and compare it to the subspecies and Loebmann, 2016). An Atlantic coast northeastern of A. fuliginosa, mostly because of the lack of collection corridor during the Pliocene–Pleistocene can be a permits and absence of good photographic equipment. possible dispersal route for A. fuliginosa from the The individual has a more melanistic colour pattern (Fig. eastern Amazon to the Atlantic forest as demonstrated 1) similar to the population of A. f. wiedi from Santa for amphibians (Fouquet et al., 2012) and lizards (Prates Maria, in southern Bahia State (see Plate 2, Figs. 9–10 et al., 2017). in Vanzolini, 1951). The Cerrado populations have a Figure 2. Geographic distribution map of Amphisbaena fuliginosa. Records based on Chalkidis, 2000; Chalkidis et al. 2002; Vanzolini, 2002, Lemos and Facure, 2007; Silveira, 2007; Nogueira-Costa et al. 2013. A. f. amazonica (green triangles); A. f. bassleri (light blue crosses), A. f. varia (black squares), A. f. wiedi (red circles = bibliographic records; red star = this study).
First georeferenced record of Amphisbaena fuliginosa, State of Ceará, Brazil 641 Table 1. Geographic distribution of the Amphisbaena fuliginosa subspecies, with the respective coordinates and bibliographic reference. Table 1. Geographic distribution of the Amphisbaena fuliginosa subspecies, with the respective coordinates and bibliographic reference. Subespecies Locality State/Province Country Latitude Longitude Reference A. f. wiedi Açailandia Maranhão Brazil -5.783333 -47.6915 Vanzolini, 2002 A. f. wiedi Alto Paraíso Rondônia Brazil -9.616667 -63.459 Vanzolini, 2002 A. f. varia Apiaú Roraima Brazil 2.666667 -61.253167 Vanzolini, 2002 A. f. wiedi Aripuanã Mato Grosso Brazil -10.333333 -59.391667 Vanzolini, 2002 A. f. amazonica Balbina, UHE (Usina Hidroelétrica) Amazonas Brazil -1.915426 -59.517443 Vanzolini, 2002 A. f. varia Barauana, Rio, at Highway BR-210 Roraima Brazil 1.466667 -60.870333 Vanzolini, 2002 A. f. amazonica Belém Pará Brazil -1.433333 -48.488 Vanzolini, 2002 A. f. amazonica Berurí Amazonas Brazil -3.9 -61.3735 Vanzolini, 2002 A. f. wiedi Canindé, Rio Gurupí Pará Brazil -2.55 -46.522833 Vanzolini, 2002 A. f. amazonica Cucuí Amazonas Brazil -1.216667 -66.837167 Vanzolini, 2002 A. f. varia Cujubim, Rio Catrimani Roraima Brazil 1.75 -62.286833 Vanzolini, 2002 A. f. wiedi Humaitá Amazonas Brazil -7.516667 -63.043667 Vanzolini, 2002 A. f. amazonica Itapiranga Amazonas Brazil -2.733333 -58.023 Vanzolini, 2002 A. f. wiedi Jacareacanga Pará Brazil -6.448325 -57.885281 Vanzolini, 2002 A. f. wiedi km 1 Highway RO-399 Rondonia Brazil -12.7 -60.192833 Vanzolini, 2002 A. f. wiedi km 5 Highway RO-399 Rondonia Brazil -12.733333 -60.276167 Vanzolini, 2002 A. f. wiedi km 93 Highway BR-010 Pará Brazil -2.2 -47.572333 Vanzolini, 2002 A. f. wiedi Kukoinhokren, Serra de Pará Brazil -7.833333 -51.927333 Vanzolini, 2002 A. f. amazonica Manaus Amazonas Brazil -3.116667 -60.0065 Vanzolini, 2002 A. f. varia Maracá, Ilha de, Rio Uraricoera Roraima Brazil 3.416667 -61.669333 Vanzolini, 2002 A. f. wiedi Mesa, Serra da Goiás Brazil -14.25 -48.592667 Vanzolini, 2002 A. f. wiedi Oriximiná Pará Brazil -1.766667 -55.855167 Vanzolini, 2002 A. f. varia Pacaraima, Vila (border-marker BV-8) Roraima Brazil 4.5 -61.152 Vanzolini, 2002 A. f. wiedi Piracanjuba Goiás Brazil -17.3 -49.027 Vanzolini, 2002 A. f. wiedi Porto Walter Acre Brazil -8.266667 -72.742 Vanzolini, 2002 A. f. wiedi Santa Barbara Rondonia Brazil -9.166667 -63.075667 Vanzolini, 2002 A. f. wiedi Santa Maria Eterna Bahia Brazil -15.85 -39.4265 Vanzolini, 2002 A. f. amazonica Tabatinga Amazonas Brazil -4.233333 -69.924 Vanzolini, 2002 A. f. wiedi Tarauacá Acre Brazil -8.166667 -70.776667 Vanzolini, 2002 A. f. varia Tepequém Roraima Brazil 3.75 -61.7525 Vanzolini, 2002 A. f. wiedi Tomé Açu Pará Brazil -2.4 -48.156 Vanzolini, 2002 A. f. wiedi Vista Alegre, Rio Negro Amazonas Brazil -0.406526 -64.463788 Vanzolini, 2002 A. f. wiedi Cumari Goiás Brazil -18.263056 -48.151111 Lemos & Facure, 2007 A. f. varia village of Santa Rosa, Santarém Pará Brazil -2.433333 -54.7 Chalkidis, 2000 A. f. fuliginosa Amana Sustainable Development Amazonas Brazil -2.701333 -64.618306 Chalkidis, 2002 Reserve, Tefé A. f. wiedi Araguari Minas Gerais Brazil -18.5575 -48.0675 Nogueira-Costa et al.2013 A. f. wiedi João Pinheiro Minas Gerais Brazil -17.761056 -46.194306 Silveira, 2007 A. f. fuliginosa Laranjal do Jari Amapá Brazil 0.578314 -52.326769 Costa-Campos et al. 2014 A. f. wiedi Viçosa do Ceará Ceará Brazil -3.428 -41.184 this study A. f. bassleri Avila Napo Ecuador -0.633333 -77.421 Vanzolini, 2002 A. f. varia Baños Pastaza Ecuador -1.4 -78.421167 Vanzolini, 2002 A. f. varia Bucay Guayas Ecuador -2.166667 -79.122167 Vanzolini, 2002 A. f. bassleri Canelos Pastaza Ecuador -1.583333 -77.738167 Vanzolini, 2002 A. f. varia Daule, Rio Guayas Ecuador -2.166667 -79.869667 Vanzolini, 2002 A. f. varia Guayaquil Guayas Ecuador -2.166667 -79.869667 Vanzolini, 2002 A. f. varia Loja Loja Ecuador -4 -79.173667 Vanzolini, 2002 A. f. bassleri Loreto Napo Ecuador -0.633333 -77.3185 Vanzolini, 2002 A. f. bassleri Pastaza, Rio Pastaza Peru -4.916667 -76.407833 Vanzolini, 2002 A. f. varia Peña Lisa Chocó Colombia 5.01 -76.625 Vanzolini, 2002 A. f. varia Pichilingue Los Rios Ecuador -1.1 -79.468667 Vanzolini, 2002
642 Igor Joventino Roberto et al. Table 1. Continued. Subespecies Locality State/Province Country Latitude Longitude Reference A. f. varia Riobamba Chimborazo Ecuador -1.666667 -78.655 Vanzolini, 2002 A. f. varia Santo Domingo de los Colorados Pichincha Ecuador -1.083333 -79.487333 Vanzolini, 2002 A. f. bassleri Turula, Rio Upano Morona – Ecuador -2.216667 -78.189167 Vanzolini, 2002 Santiago A. f. bassleri Charobamba La Paz Bolivia -14.616667 -68.744167 Vanzolini, 2002 A. f. bassleri Sorata La Paz Bolivia -15.783333 -68.677667 Vanzolini, 2002 A. f. bassleri Tipuani La Paz Bolivia -15.55 -68.011167 Vanzolini, 2002 A. f. bassleri Yungas La Paz Bolivia -16.166667 -67.511333 Vanzolini, 2002 A. f. varia Andagoya Chocó Colombia 5.1 -76.675 Vanzolini, 2002 A. f. varia Barrancabermeja Santander Colombia 7.05 -73.87 Vanzolini, 2002 A. f. varia Honda Tolima Colombia 5.2 -74.751667 Vanzolini, 2002 A. f. varia Las Animas, Caño Chocó Colombia 5.333333 -76.725 Vanzolini, 2002 A. f. amazonica Leticia Amazonas Colombia -4.15 -69.957167 Vanzolini, 2002 A. f. varia Medellin Antioquia Colombia 6.25 -75.608333 Vanzolini, 2002 A. f. varia Muzo Boyacá Colombia 5.533333 -74.113333 Vanzolini, 2002 A. f. varia Paime Cundinamarca Colombia 5.366667 -74.181667 Vanzolini, 2002 A. f. varia Peña Lisa Chocó Colombia 5.01 -76.625 Vanzolini, 2002 A. f. varia Rio Frio Magdalena Colombia 10.9 -74.185 Vanzolini, 2002 A. f. varia San Pedro Valle del Cauca Colombia 4 -76.219 Vanzolini, 2002 A. f. varia Villavicencio Meta Colombia 4.15 -73.618833 Vanzolini, 2002 A. f. fuliginosa Christiaankondre Suriname 5.716667 5.716667 Vanzolini, 2002 A. f. fuliginosa Georgetown Guyana 6.783333 -58.188333 Vanzolini, 2002 A. f. fuliginosa Kaieteur Falls Guyana 5.166667 -59.4685 Vanzolini, 2002 A. f. fuliginosa Kalacoon Guyana 6.383333 -58.64 Vanzolini, 2002 A. f. fuliginosa Kamakusa Guyana 5.933333 -59.91 Vanzolini, 2002 A. f. fuliginosa Maccasseema Guyana 7.25 -58.718333 Vanzolini, 2002 A. f. fuliginosa Marudi River Guyana 2.116667 -59.57 Vanzolini, 2002 A. f. fuliginosa Nappi, Kanuku Mts. Guyana 3.416667 -59.5695 Vanzolini, 2002 A. f. fuliginosa Paramaribo Suriname 5.083333 -55.173333 Vanzolini, 2002 A. f. fuliginosa Saint Laurent du Maroni French Guiana 5.5 -54.040333 Vanzolini, 2002 A. f. bassleri Boca Santiago Amazonas Peru -4.45 -77.640833 Vanzolini, 2002 A. f. bassleri Cashiboya Loreto Peru -6.85 -74.741667 Vanzolini, 2002 A. f. bassleri Rio Cenipa Amazonas Peru -4.65 -78.174333 Vanzolini, 2002 A. f. bassleri Contamana Loreto Peru -7.333333 -75.041833 Vanzolini, 2002 A. f. bassleri Cushabatay, Rio Loreto Peru -7.15 -75.141833 Vanzolini, 2002 A. f. bassleri Iquitos Loreto Peru -3.787267 -73.223333 Vanzolini, 2002 A. f. bassleri Pampa Hermosa Loreto Peru -7.2 -75.3085 Vanzolini, 2002 A. f. bassleri Pucallpa Ucayali Peru -8.383333 -74.558833 Vanzolini, 2002 A. f. bassleri Reforma Loreto Peru -6.733333 -74.975 Vanzolini, 2002 A. f. bassleri Reforma Loreto Peru -5.06875 -73.891333 Vanzolini, 2002 A. f. bassleri Roaboya Loreto Peru -7.8 -74.775167 Vanzolini, 2002 A. f. bassleri San Gaban, Rio Puno Peru -13.416667 -70.305 Vanzolini, 2002 A. f. varia Panamá city Panamá 9.012081 -79.548144 Vanzolini, 2002 A. f. varia Frijoles Panamá 9.173888 9.173888 Vanzolini, 2002 A. f. varia Barro Colorado Panamá 9.173888 -79.847094 Vanzolini, 2002 A. f. varia Monte lirio Panamá 8.795141 -82.804762 Vanzolini, 2002 A. f. varia Gatun Panamá 9.2709 -79.909061 Vanzolini, 2002 A. f. varia Chagres River Panamá 9.281204 -79.476275 Vanzolini, 2002 A. f. varia Canal Zone Panamá 9.130613 -79.740784 Vanzolini, 2002 A. f. varia Bohio Panamá 8.956241 -79.549046 Vanzolini, 2002
First georeferenced record of Amphisbaena fuliginosa, State of Ceará, Brazil 643 Acknowledgments. We acknowledge the financial assistance of Nogueira-Costa, P., Aguiar, F.V.O., da Silva, G.R., Afonso, M.C., Conselho Nacional de Desenvolvimento Científico e Tecnológico Baldine, J.T.B., Venâncio, M.F. (2013): Reptilia, Squamata, (CNPq) for a postdoctoral fellowship to IJR (PDJ 159999/2019- Amphisbaenidae, Amphisbaena fuliginosa wiedi Vanzolini, 7) and research fellowships to RWA (PQ# 303622 / 2015-6, 1951: distribution extension. Check List 9(1): 167–168. 305988 / 2018-2). María Camila Vallejo-Pareja and Marcelo Prates, I., Rivera, D., Rodrigues, M.T., Carnaval, A.C. (2016): Menin reviewed earlier drafts of this manuscript and assisted A mid-Pleistocene rainforest corridor enabled synchronous with the English. invasions of the Atlantic Forest by Amazonian anole lizards. Molecular Ecology 25: 5174–5186. References Roberto, I.J., Loebmann, D. (2016): Composition, distribution patterns, and conservation priority areas for the herpetofauna Costa, H.C.C., Bérnils, R.S. (2018): Répteis do Brasil e suas of the state of Ceará, northeastern Brazil. Salamandra 52(2): unidades federativas: lista de espécies. Herpetologia Brasileira 134–152. 7(1): 11–57. Vanzolini, P.E. (1951): Contributions to the knowledge of the Fouquet, A., Loebmann, D., Castroviejo-Fisher, S., Padial, J.M., Brazilian lizards of the family Amphisbaenidae Gray, 1825. Orrico, V.G.D., Lyra, M.L., et al. (2012): From Amazonia to the 6. On the geographical distribution and differentiation of Atlantic Forest: molecular phylogeny of Phyzelaphryninae frogs Amphisbaena fuliginosa Linné. Bulletin of the Museum of reveals unexpected diversity and a striking biogeographic pattern Comparative Zoology 106: 1–67. emphasizing conservation challenges. Molecular Phylogenetics Vanzolini, P.E. (2002): A second note on the geographical and Evolution 65: 547–561. differentiation of Amphisbaena fuliginosa L., 1758 (Squamata, Lemos, F.G., Facure, K.G. (2007): New record of Amphisbaena Amphisbaenidae), with a consideration of the forest refuge fuliginosa (Squamata, Amphisbaenidae) for the Cerrado biome, model of speciation. Anais da Academia Brasileira de Ciências in an area of extensive cattle ranching. Biota Neotropica 7(1): 74(4): 609–648. 239–241. Loebmann, D., Haddad, C.F.B. (2010): Amphibians and reptiles from a highly diverse area of the Caatinga domain: composition and conservation implications. Biota Neotropica 10(3): 227– 256. Accepted by Timothy Colston
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