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Research Article
A new species of Amphisbaena (Squamata: Amphisbaenidae) from the Orinoquian region of Colombia
expand article infoJuan José Torres-Ramírez‡§, Teddy Angarita-Sierra|‡, Mario Vargas-Ramírez§
‡ Fundación de Investigación en biodiversidad y conservación, Bogotá, Colombia
§ Universidad Nacional de Colombia, Bogotá, Colombia
| Universidad Manuela Beltrán, Bogotá, Colombia

Corresponding author: Teddy Angarita-Sierra ( tgangaritas@unal.edu.co )

Academic editor: Uwe Fritz
© 2021 Juan José Torres-Ramírez, Teddy Angarita-Sierra, Mario Vargas-Ramírez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Torres-Ramírez JJ, Angarita-Sierra T, Vargas-Ramírez M (2021) A new species of Amphisbaena (Squamata: Amphisbaenidae) from the Orinoquian region of Colombia. Vertebrate Zoology 71: 55-74. https://doi.org/10.3897/vz.71.e59461
ZooBank: urn:lsid:zoobank.org:pub:EC812295-41EF-4D78-8FCD-CFB2A45DC359
Open Access

Abstract

In northern South America, amphisbaenians are rarely seen among the herpetofauna.Thus, general knowledge about them is very poor. During a herpetological survey in 2012 at Casanare, Colombia, we found two specimens of an unusual Amphisbaena. A third specimen sharing the same morphotype labeled Amphisbaena sp. from Vichada department was found deposided in an Colombian reptile collection. Based on morphological analyses together with phylogenetic analyses of 1029 base pairs of the mitochondrial DNA (mtDNA), we describe a new species of Amphisbaena that inhabits in the Orinoquian region of Colombia. The new species is part of a phylogenetic clade together with A. mertensii and A. cunhai (central-southern Brazil), exhibiting a great genetic distance (26.1–28.9%) between the newly identified lineage versus those taxa, and versus the sympatric taxa A. alba and A. fuliginosa. Morphologically, this new Amphisbaena can be distinguished from their congeners by characters combination of number of preocloacal pores, absence of malar scale, postgenial scales and body and caudal annuli counts. Amphisbaena gracilis is on morphology grounds the most similar species. However, the new species can be distinguished from it by having higher body annuli counts, angulus ories aliegned with the edges of the ocular scales and center of frontal scales, less number of large middorsal segments of the first and second body annulus, and rostral scale visible from above. The description of this new Amphisbaena species points out the urgent need to increase the knowledge of worm lizards in Colombia

Keywords

burrowing habits, cryptic species, fossorial, integrative taxonomy, mtDNA, worm lizard, South America

Introduction

Amphisbaenians are one of the most enigmatic and unusual squamates. All species have burrowing habits, but some occasionally venture onto the surface or can be found under objects on the ground (Pough et al. 1998). Thus, due to its fossorial habit, cryptic behavior, secretive microhabitats and lower encounter rate, amphisbaenians are considered an elusive research objective. About 102 species of the genus Amphisbaena Linnaeus, 1758 have been described in South America (Gans 2005; Uetz et al. 2020), with Brazil being the country with the highest diversity with over 80 species (Gans 2005; Gomes and Maciel 2012; Teixeira et al. 2014; Uetz et al. 2020).

Since Gans and Mathers (1977) early efforts to establish species boundaries between Amphisbaena from northern South America (sensu Eva and Huber 2005), few researchers have focused on continuing studies on the zoogeography and systematics of these uncommon reptiles (Costa et al. 2018b). The Northern South American Amphisbaena currently comprise eight nominal species: A. alba Linnaeus, 1758; A. fuliginosa Linnaeus, 1758; A. medemi Gans & Mathers, 1977; A. spurrelli Boulenger, 1915; A. gracilis Strauch, 1881; A. rozei Lancini, 1963; A. stejnegeri Ruthven, 1922 and A. vanzolinii Gans, 1963; all inhabiting the tropical lowland ecosystems of Panama, Colombia, Venezuela, Guyana and Surinam.

Colombia is considered to be a megadiverse country in part due to its rich fauna of around 621 species of reptiles (Uetz et al. 2020). However, worm lizards remain poorly represented in the Colombian herpetofauna due to the lack of scientific knowledge. Currently, Colombian worm lizards comprise two genera (Mesobaena Mertens, 1925 and Amphisbaena Linnaeus, 1758) and five species: Mesobaena huebneri Mertens, 1925; Amphisbaena alba, A. fuliginosa, A. medemi and A. spurrelli. Amphisbaena alba and A. fuliginosa (sensu Vanzolini 2002) are the most widely distributed amphisbeanids in the country; A. alba is restricted to the Cis-Andean region while A. fuliginosa is present in both Cis and Trans-Andean regions, ranging from the sea level to 1300 m. a.s.l. Amphisbaena spurrelli was the first amphisbeanid described in Colombia. It is distributed across the Chocoan region to Panáma and its type locality corresponds to corregimiento of Andagoyá, Municipality of San Juan, department of Chocó (Boulenger 1915; Gans and Mathers 1977). Mesobaena huebneri, the second worm lizard species described, is only known from three disjunct and distant localities: Its type locality corresponds to department of Inirida (Amazonian basin, specific locality unknown); the Timbá community, municipality of Mitu, deparment of Vaupes; and Serranía de la Macarena, department of Meta [specific locality unknown (Gans 1971; Cole and Gans 1987)]. Finally, Amphisbaena medemi was erected by Gans and Mathers 33 years ago and is the most recently described worm lizard. This species is distributed across the Caribbean region of Colombia, having as type locality the old Inderena fishing facility at Ciénaga de Amajehuevo, municipality of San Cristobal, Atlántico.

After the early efforts made by Gans and collaborators during the 20th century, few attempts have been made to carry out a comprehensive taxonomic assessment of the Amphisbaena species distributed in Colombia, as well as in northern South America (Señaris 1999; Costa et al. 2018a). The most recent studies in Colombia have only provided a check list of the already known Amphisbaena species or distributional records obtained from fieldwork, ignoring the specimens housed in museums that are waiting for a detailed revision (Rangel-Ch et al. 2012; Angarita-Sierra et al. 2013; Aponte-Gutiérrez et al. 2019; Carvajal-Cogollo 2019).

During a herpetological inventory in the department of Casanare, Colombia (Pedroza-Banda et al. 2014), we found two specimens of an unusual Amphisbaena from the municipalities of Paz de Ariporo and Orocué. A third specimen sharing the same morphotype seen in the Amphisbaena specimens from Casanare was found in the reptile collection of the Pontificia Universidad Javeriana, labeled as Amphisbaena sp., from the municipality of Puerto Carreño, department of Vichada. These three specimens shared unique similarities between them and did not match previous descriptions of any recognized species of the genus (Gonzalez-Sponga and Gans 1971; Gans and Mathers 1977; Gans 2005). Hence, it has become clear that these specimens represent an undescribed evolutionary lineage of amphisbaenians. Therefore, the goal of this paper is to recognize this new species and describe it by integrating molecular and morphological analyses.

Methods

Ethics statement

Fieldwork was performed under the scientific research permit for collection of wild specimens of biological diversity for non-commercial purpose issued by CORPORINOQUIA (Research Auto: 500.5712.0380) and the Colombian Ministry of Environment and Sustainable development (MADS) by agreement 083 of 2012. This study was conducted following the Colombian animal welfare law and the collection of wild specimens of the biological diversity acts (Ley 1774, 2016; Decreto 1376, 2013), as well as considering the Universal Declaration on Animal Welfare (UDAW) endorsed by Colombia in 2007.

Fieldwork and sampling

Fieldwork was carried out in August 2012 in the municipalities of Paz de Ariporo and Orocué, department of Casanare, Colombia. Searches for amphisbaenians were conducted by three researchers from 8:00 to 11:30 and 14:00 to 17:00 for 15 days, with a sampling effort of 97.5 man/hours. We removed covered objects and leaf litter, digging up the ground from 5 to15 cm deep, during three to five minutes for each event. Particularly, we included piles of palm leaves of moriche palm (Mauritia flexuosa L.f., 1782), as part of the microhabitats sampled. Individuals collected were immediately placed into cloth bags for later general procedures of measurement and identification as described by Pedroza-Banda et al. (2014).

Molecular data collection and laboratory procedures

Molecular distinctiveness and phylogenetic relationships of the new species of Amphisbaena were assessed by analyzing molecular data corresponding to 1029 bp of the NADH dehydrogenase subunit 2 (ND2) gene, mtDNA. We assembled a data set by aligning the sequence from the new species and colombian individuals of A. alba and A. fuliginosa, with homologous sequences from the Antillean and South American amphisbaenian species published in Genbank (Table 1). The homologous ND2 sequence of the lizard species Anolis auratus DQ377355 was used as outgroup. Total genomic DNA was extracted using a standard phenol-chloroform method (Sambrook et al. 1989). We amplified the gene fragment using the primer pairs NADHF/NADH R and L4349/H5540 (Measey and Tolley 2013). We carried out PCRs in a total volume of 30 μl containing one-unit Taq polymerase (Bioline; Randolph, MA), 1 X of buffer (Bioline), a final concentration of 1.5 mM MgCl2 (Bioline), 0.5 μM of each primer, 0.2 mM of each dNTP (Bioline), 0.2 µg of bovine serum albumin (BSA) and approximately 50 ng of total DNA. We purified the PCR products using the ammonium acetate protocol (Bensch et al. 2000), and we sequenced them on an ABI 3130xl genetic analyzer (Applied Biosystems, Foster City, CA, USA) using the BigDye Terminator v3.1 Cycle Sequencing Kit (Applied Biosystems) at the Instituto de Genética, Universidad Nacional de Colombia. We stored the remaining DNA extractions at –80°C in the tissue collection of the Instituto de Genética (for voucher numbers see Table 1). We performed the thermocycling conditions as indicated by Measey and Tolley (2013). The GenBank accession numbers of the obtained sequences are: MT433762, MT433763, MT433764, MT433765, MT433766 (Table 1). The sequences were edited and aligned using Chromas 1.51 (http://www.technelysium.com.au/chromas.html) and BioEdit 7.0.5.2 (Hall 1999).

Table 1.
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ND2 sequences of Amphisbaena species used in the present study.

Species Locality Accession number. ND2 Voucher Source
A. alba Brazil: Vilhena, Rondônia FJ441943 CHUNB 12795 Mott and Vieites 2009
A. alba Brazil: Jalapão, Tocantins FJ441948 CHUNB 30678 Mott and Vieites 2009
A. alba Brazil: Minaçu, Goiás FJ441946 CHUNB 430 Mott and Vieites 2009
A. alba Brazil: Minaçu, Goiás FJ441947 CHUNB 435 Mott and Vieites 2009
A. alba Brazil: Mariana, Minas Gerais FJ441941 JC 795a Mott and Vieites 2009
A. alba Brazil: Uruçuí-Una, Piauí FJ441942 MTR 5502a Mott and Vieites 2009
A. alba Brazil: Manso, Mato Grosso FJ441940 MZUSP 88618 Mott and Vieites 2009
A. alba Brazil: Lajeado, Tocantins FJ441944 MZUSP 94813 Mott and Vieites 2009
A. alba Brazil: Guarantã do Norte, Mato Grosso FJ441949 UFMT 3468 Mott and Vieites 2009
A. alba Brazil: Campo Novo dos Parecis, Mato Grosso FJ441945 UFMT 3476 Mott and Vieites 2009
A. alba Colombia: Paz de Ariporo, Casanare MT433762 MLS 1904 This study
A. anaemariae Brazil: Brasília, Distrito Federal FJ441911 CHUNB 38647 Mott and Vieites 2009
A. angustifrons Argentina: Tucuman FJ441950 Monteiro 3 Mott and Vieites 2009
A. anomala Brazil:Igarapé-Açú, Pará FJ441955 MPEG 22139 Mott and Vieites 2009
A. anomala Brazil: Sao Antônio de Tauá, Pará FJ441956 MPEG 22141 Mott and Vieites 2009
A. arenaria Brazil: Canudos, Bahía KY018695 MTR23279 Teixeira et al. 2016
A. bahiana Brazil: Campo Formoso, Bahía MG028575 MZUSP106222 Dal Vechio et al. 2018
A. bahiana Brazil: Campo Formoso, Bahía MG028574 MZUSP106221 Dal Vechio et al. 2018
A. bolivica Argentina: Tucuman FJ441913 Monteiro 11 Mott and Vieites 2009
A. bolivica Argentina: Salta FJ441912 Monteiro 8 Mott and Vieites 2009
A. brasiliana Brazil: Guarantã do Norte, Mato Grosso FJ441951 UFMT3998 Mott and Vieites 2009
A. caeca USA: Manati, Puerto Rico FJ441914 MVZ 232753 Mott and Vieites 2009
A. caiari Brazil: Porto Velho, Rondônia KJ669333 MZUSP101602 Teixeira et al. 2014
A. caiari Brazil: Porto Velho, Rondônia KJ669334 MZUSP104237 Teixeira et al. 2014
A. camura Brazil: Aquidauana, Mato Grosso do Sul FJ441915 MPEG 21463 Mott and Vieites 2009
A. carli Brazil: Sao Desiderio, Bahia KY352335 MTR17848 Teixeira et al. 2016
A. cuiabana Brazil: Campo Novo dos Parecis, Mato Grosso FJ441938 UFMT 3545 Mott and Vieites 2009
A. cuiabana Brazil: Campo Novo dos Parecis, Mato Grosso FJ441939 UFMT 3546 Mott and Vieites 2009
A. cunhai Brazil: Manaus, Amazonas FJ441916 LSUMZH13969 Mott and Vieites 2009
A. darwinii Brazil: São Jerônimo, Rio Grande do Sul FJ441936 MCP 14723 Mott and Vieites 2009
A. elbakyanae sp. nov. Colombia: Paz de Ariporo, Casanare MT433763 MLS 1901 This study
A. fuliginosa Brazil JN700169 BPN 988 Genbank
A. fuliginosa Brazil: Manso, Mato Grosso FJ441926 MTR 3177 Mott and Vieites 2009
A. fuliginosa Brazil: Aripuanã, Mato Grosso FJ441927 MZUSP 82798 Mott and Vieites 2009
A. fuliginosa Peru: San Jacinto, Loreto FJ441925 KU 222189 Mott and Vieites 2009
A. fuliginosa Colombia: San Martín, Meta MT433765 MLS 1903 This study
A. fuliginosa Colombia: Bucaramanga, Santander MT433764 UIS-R 3181 This study
A. fuliginosa Colombia: Girón, Santander MT433766 UIS-R 3724 This study
A. hastata Brazil: Mocambo do Vento, Bahia FJ441920 MTR 3555 Mott and Vieites 2009
A. hastata Brazil: Mocambo do Vento, Bahia FJ441921 MTR 3662 Mott and Vieites 2009
A. ignatiana Brazil: Santo Inácio, Bahia FJ441922 MTR 3538 Mott and Vieites 2009
A. ignatiana Brazil: Santo Inácio, Bahia FJ441923 MZUSP 93480 Mott and Vieites 2009
A. kingii Brazil: São Jerônimo, Rio Grande Do Sul FJ441969 MCP 14720 Mott and Vieites 2009
A. kingii Brazil: São Jerônimo, Rio Grande Do Sul FJ441968 MCP 14721 Mott and Vieites 2009
A. kraoh Brazil: Jalapão, Tocantins FJ441935 CHUNB 30676 Mott and Vieites 2009
A. leeseri Brazil: Mateiros, Tocantins FJ441937 CHUNB 41351 Mott and Vieites 2009
A. leucocephala Brazil: Santa Maria Eterna, Bahia KY352337 MTR33126 Teixeira et al. 2016
A. leucocephala Brazil: Ilheus, Bahia KY352336 MTR33467 Teixeira et al. 2016
A. mertensii Paraguay: Itapua, Alto Vera FJ441917 KU 290721 Mott and Vieites 2009
A. mertensii Brazil: Marília, Sao Paulo FJ441919 MPEG 21462 Mott and Vieites 2009
A. mertensii Brazil: Campo Novo dos Parecis, Mato Grosso FJ441918 UFMT 3469 Mott and Vieites 2009
A. mitchelli Brazil: Belo Monte, Alagoas KY018696 BM137 Teixeira et al. 2016
A. munoai Brazil: São Jerônimo, Rio Grande Do Sul FJ441930 MCP 14749 Mott and Vieites 2009
A. pretrei Brazil: EEEWG, Bahia KY352338 MTR22216 Teixeira et al. 2016
A. pretrei Brazil: Salvador, Bahia KY352339 TM262 Teixeira et al. 2016
A. roberti Brazil: Lajeado, Tocantins FJ441954 MTR 6770 Mott and Vieites 2009
A. roberti Brazil: Marilia MG028576 TM16 Dal Vechio et al. 2018
A. saxosa Brazil: Lajeado, Tocantins FJ441952 MTR 8830 Mott and Vieites 2009
A. saxosa Brazil: Lajeado, Tocantins FJ441953 MTR 8831 Mott and Vieites 2009
A. schmidti USA: Puerto Rico AY605475 MVZ 232754 Macey et al. 2004
A. schmidti USA: PuertoRico, Marchiquita NC_006284 MVZ 232754 Macey et al. 2004
A. schmidti USA, Manati, Puerto Rico FJ441924 MVZ 232756 Mott and Vieites 2009
A. silvestrii Brazil, Cuiabá, Mato Grosso FJ441931 UFMT 3996 Mott and Vieites 2009
A. silvestrii Brazil, Cuiabá, Mato Grosso FJ441932 UFMT 3997 Mott and Vieites 2009
A. uroxena Brazil, Mucuge, Bahia MG028577 MZUSP95987 Dal Vechio et al., 2018
A. uroxena Brazil, Mucuge, Bahia MG028578 MZUSP95988 Dal Vechio et al., 2018
A. vermicularis Brazil, Paranã, Tocantins FJ441928 CHUNB 35348 Mott and Vieites 2009
A. vermicularis Brazil, Paranã, Tocantins FJ441929 CHUNB 35349 Mott and Vieites 2009
A. vermicularis Brazil, Alagoado, Bahia MG028579 MTR11246 Dal Vechio et al. 2018
A. vermicularis Brazil, Santo Inacio, Bahia MG028583 MTR11294 Dal Vechio et al. 2018
A. vermicularis Brazil, Serra do Cipo, Minas Gerais MG028580 MTR20286 Dal Vechio et al. 2018
A. vermicularis Brazil, Lajeado, Tocantins MG028582 LAJ403 Dal Vechio et al. 2018
A. xera — AY662541 — Townsend et al. 2004
Amphisbaena sp. Brazil, Pacoti, Ceara FJ441933 MTR 169 Mott and Vieites 2009
Amphisbaena sp. Brazil, Serra das Confusões, Piauí FJ441934 SC 76 Mott and Vieites 2009

Phylogenetic analyses and genetic divergence

We analyzed the dataset using the unpartitioned and partitioned (i.e., we treated each codon of the protein-coding gene ND2 as distinct partitions) partition schemes. We assessed the optimal partitioning scheme and best-fit evolutionary models using Partitionfinder v1.1.1 and the Bayesian Information Criterion (Lanfear et al. 2012), resulting in the selection of the partitioned scheme. For this scheme we applied the resulting models in a Bayesian analysis with MrBayes v3.2.1 (Ronquist et al. 2012): ND2 1st and 3rd codons – GTR+I+G and ND2 2nd codon – TVM+G. We incorporated these models into a single tree search mixed model partitioning approach (Nylander et al. 2004). For this analysis, we carried out two parallel runs using four Markov chains, each starting from a random tree. We ran the Markov chains for 20 million generations. The burn-in was set to sample only the plateau of the most likely trees that were used for generating a 50% majority-rule consensus. We then used the software TRACER 1.5.4 (Rambaut and Drummond 2007) to assess an acceptable level of the MCMC chain mixing and to estimate effective sample sizes for all parameters. To assess the genetic differentiation between the new lineage and the other related Amphisbaena species (including the sympatric ones A. fuliginosa and A. alba), we calculated uncorrected p genetic distances for the ND2 gene fragment using MEGA 7.0.21 (Kumar et al. 2016).

Morphology

We compared the collected amphisbaenians and the individual found in the collection of the Pontificia Universidad Javeriana to other preserved specimens housed in the following colombian biological collections: reptile collection of the Instituto de Ciencias Naturales, Universidad Nacional de Colombia (ICN-R, Bogotá); Museo de Historia Natural, Universidad de Antioquia (MHUA, Medellin); Museo de la Universidad La Salle (MLS, Bogotá); Pontificia Universidad Javeriana (MUJ, Bogotá); Instituto de Investigación de Recursos Biológicos Alexander von Humboldt (IAvH-R, Villa de Leyva) and the reptile collection of the Universidad Industrial de Santander (UIS-R, Bucaramanga).

We compared the pholidosis of the three specimens analyzed in this study to morphological data available in published references of the 50 nominal four pored Amphisbaena species, as well as to the Amphisbaena species that inhabit the Orinoquian region (Table 2). The definition and terminology used in the diagnosis, description and comparison sections are, as far as possible, in accordance with the broadly used descriptions of South American amphisbaenians according to Gans (1962, 1963, 1967); Gans and Mathers (1977); Vanzolini (1994); Vanzolini (2002); Teixeira et al. (2014) as follows: number of precloacal pores (P); supralabial scales (SS); infralabial scales (IS); temporal scales (TS); number of segments of the first postgenial scale row (FPG); number of segments of the second postgenial scale row (SPG); malar scales (M); number of segments of the postmalar scale row (PM); body annuli (BA); caudal annuli (CA); number of dorsal segments per annulus at midbody (DS); number of ventral segments per annulus at midbody (VS); number of segments per annulus at anterior edge of the cloaca (SAC); number of segments per annulus at posterior edge of the cloaca (SPC); number of cloacal annuli (CCA) [Cloaca annuli are those between the anterior and posterior edge of the cloaca]; autotomy sites on caudal annuli (AUC). Likewise, we followed the characters used by Gonzalez-Sponga and Gans (1971), particularly, we added to our analyses the angulus oris (i.e. the lateral limit of the oral fissure formed by junction of upper and lower lips), as well as the presence/absence or number of the large middorsal segments of the first and second body annulus.

Table 2.
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Pholidosis comparisons between Amphisbaena elbakyanae sp. nov. and all the four-pored Amphisbaena species from South America.

Species P Head scales Body and caudal scales Source
SS IS TS FPG SPG M PM BA CA DS VS SAC SPC CCA AUC
A. elbakyanae sp. nov. 4 3 3 2–3 4 0 0 6–7 245–257 20–24 13–15 16–18 6–7 11–12 4 6–8 *
A. alba Linnaeus, 1758 4–10 4 3 5 2 2–3 1 12–15 198–248 13–21 30–42 35–46 10 Absent 1, 2, 3, 4, 5, 6
A. albocingulata Boettger, 1885 4 3 3 0 183–204 23–27 12–14 15–18 7–9 4, 5, 7, 8
A. angustifrons Cope, 1861 3–6 4 3 P 190–253 12–18 20–31 21–30 Absent 4, 5, 9
A. arda Rodrigues, 2003 4 4 3 1 P 242 30 23 23 8 5, 10
A. arenaria Vanzolini, 1991 4 3 3 P P 0 285–307 22–23 12–14 14–16 6–7 4, 5, 6, 11, 12
A. arenicola Perez & Borges-Martins, 2019 4 3–4 3 2 2 3 1 6 199–216 20–22 12–14 15–18 6 11 8–9 8
A. bahiana Vanzolini, 1964 4 3 3 204–223 14–16 12–16 14–20 4–5 5, 13
A. bedai Vanzolini, 1991 4 4 3 P 272–284 22–23 18–20 16–18 6 5, 14
A. bolivica Mertens, 1929 2–6 3 3 200–231 18–26 27–36 26–36 3–5 4, 5, 6, 15, 16
A. borelli Peracca, 1897 4 3 3 239–245 17–19 14–16 16–20 6–8 5, 17
A. brasiliana Gray, 1865 4 3 3 213–229 11–15 18–21 18–22 Absent 5, 6, 18, 52
A. camura Cope, 1862 3–6 4 3 188–207 14–19 28–42 29–46 3–5 4, 5, 6, 19,
A. carvalhoi Gans, 1965 4 3 3 0 231–245 19–22 12–14 16–18 7–8 4, 5, 20
A. cegei Montero, Sáfadez & Álvarez, 1997 4 3 3 3 4–5 1 0 179–199 22 17–22 17–23 6 13–15 3–4 6–8 4, 5, 21, 22
A. cuiabana Strussman & Carvalho, 2001 4 3 3 286–292 18–20 14 16 9–10 5, 23
A. cunhai Hoogmoed & Ávila-Pires, 1991 4 3 3 2 2–3 0 1 7–9 226–239 25–26 14–16 14–18 6 7–11 5–7 4, 5, 6, 24
A. darwinii Duméril & Bibron, 1839 2–5 3 3 P 174–199 18–25 13–19 16–23 7–10 4, 5, 8, 25, 26
A. frontalis Vanzolini, 1991 4 3 3 0 252–272 23–24 14–16 14–16 6–7 4, 5, 11
A. fuliginosa Linnaeus, 1758 6–9 2–3 3–4 3–5 2–6 5–7 1–2 10–14 196–218 24–30 19–28 21–28 7–10 10–16 3–6 4–7 1, *
A. gracilis Strauch, 1881 4 3 3 2 4 0 0 7–8 224–248 21–24 13–16 14–17 6 12–13 5 6–7 4, 27, 28, 29, 30
A. hastata Vanzolini, 1991 4 3 3 266–273 40 18 16 12–16 4, 5, 31
A. heathi Schmidt, 1936 4 3 3 0 183–187 32 12 18–20 7–8 4, 5, 32
A. hogei Vanzolini, 1950 4 3 3 P 177–191 15–19 10–13 14–18 4–7 4, 5, 8, 33
A. ibijara Rodrigues, Andrade & Lima, 2003 4 3 3 1 6 6 1 0 239–250 23–25 14–16 14–16 8–11 5, 34,
A. kingii Bell, 1833 4 3 3 P P P 214–244 15–23 12–19 14–22 7 5, 35, 36
A. lumbricalis Vanzolini, 1996 2–6 3 3 0 225–247 20–26 12–16 16–20 6–10 4, 5, 26, 37
A. medemi Gans & Mathers, 1977 4 3 3 2 2–3 3–5 1 9 230–235 17–18 14–16 17–18 6–8 12–17 5–7 4, 5, 30, 38
A. munoai Klappenbach, 1960 4 3 3 2 3 0 9 194–221 18–25 10–15 13–20 6–8 7–14 5–9 4, 5, 8, 39
A. myersi Hoogmoed, 1989 4 3 3 221 28 16 16 8 4, 5, 40
A. nigricauda Gans, 1966 0/4–5 3 3 0 192–226 19–24 9–11 13–16 6–10 4, 5, 8, 41, 42
A. occidnetalis Cope, 1875 4 4 3 P 261–279 18–26 16–19 22–27 9 4, 5, 43
A. pericensis Noble, 1921 4 3 3 0 198–218 16–19 12–16 16–20 6–8 4, 5, 44
A. plumbea Gray, 1872 4 4 3 P 210–283 16–21 18–27 20–30 5–9 4, 5, 45
A. polygrammica Werner, 1901 4 3 3 P 0 270 22 18 16 – 4, 5, 36, 46
A. prunicolor Cope, 1885 4 3 3 2 2 0 1 8 180–215 18–27 10–17 14–20 7–11 4, 5, 8, 47
A. ridleyi Boulenger, 1890 4 4 3 P 172–192 14–17 16–18 20–28 Absent 4, 5, 48
A. rozei Lancini, 1963 4 4 3 2 3 0 1 7 205–209 20 15–16 14 6–7 4, 5, 30, 49, 50
A. sanctaeritae Vanzolini, 1994 4 3 3 269 12 12 6–7 5, 51
A. saxosa Castro-Mello, 2003 4 4 3 2 2 0 1 8 253–272 17–21 18–24 16–21 6 4 Absent 5, 6, 52
A. slateri Boulenger, 1907 4 3 3–4 2 2–3 2–4 1 0–7 176–213 20–24 10–14 14–16 6–8 10–12 7–10 4, 5, 36, 53, 54
A. slevini Schmidt, 1936 4 2 2 0 204–211 23–25 10–14 10–12 5–6 4, 5, 32
A. spurrelli Boulenger, 1915 4 4 4 2 2 0 1 7 213–222 18–23 16–18 16–18 6 7 4, 5, 30, 56
A. steindachneri Strauch, 1881 4 3 3 256–266 17–18 14–16 16 7 5, 57
A. stejnegeri Ruthven, 1922 6 4 2 243–247 13 17–19 16–20 6 9 4, 30, 58
A. supernumeraria Mott, Rodrigues & Dos Santos, 2009 4 3 3 0 2 3 1 0 333–337 22–23 14 17–18 10–12 5, 59
A. talisiae Vanzolini, 1995 4 3 3 2 2 0 1 P 205–234 17–29 10–14 14–18 5–8 7–14 6–8 4, 5, 60, 61
A. townsendi Stejneger, 1911 4 4 3 P 261–279 22–26 16–19 22–27 7–8 5, 62
A. trachura Cope, 1885 3–4 3 3 P 168–208 15–25 14–24 16–24 6–8 9–14 5–9 8, 25, 47, 63
A. tragorrhectes Vanzolini, 1971 4 4 3 P 169 31 12 12 12–14 4, 5, 64
A. vanzolinii Gans, 1963 4 2 2 200–231 28–31 12–16 12–18 7–14 4, 24, 30, 3
A. vermicularis Wagler, 1824 4 211–254 23–30 18–26 18–25 6 4, 6, 65
A. xera Thomas, 1966 4 3 3 0 225–234 12–16 12–16 14–16 5–7 5, 30, 55

Precloacal pores (P); supralabial scales (SS); infralabial scales (IS); temporal scales (TS); number of segments of the first postgenial scale row (FPG); number of segments of the second postgenial scale row (SPG); malar scales (M); number of segments of the postmalar scale row (PM); body annuli (BA); caudal annuli (CA); number of dorsal segments perannulus at midbody (DS); number of ventral segments per annulus at midbody (VS); number of segments per annulus at anterior edge of the cloaca (SAC); number of segments perannulus at posterior edge of the cloaca (SPC); number of cloacal annuli [(CCA) Cloaca annuli are those between anterior and posterior edge of the cloaca]; autotomy sites on caudal annuli (AUC). Source: * = This study, 1= (Linnaeus 1758), 2= (Gans 1962), 3= (Gans 1963), 4= (Vanzolini 2002), 5= (Maciel 2011), 6= (Dal Vechio et al. 2016), 7= (Boettger 1885), 8= (Perez and Borges-Martins 2019), 9= (Cope 1861), 10= (Rodrigues 2003), 11= (Vanzolini 1991b) , 12= (Teixeira et al. 2016), 13= (Vanzolini 1964), 14= (Vanzolini 1991a), 15= (Mertens 1929), 16= (Montero 2019), 17= (Peracca 1897), 18= (Gray 1865), 19= (Cope 1862), 20= (Gans 1965), 21= (Montero et al. 1997), 22= (Montero 2001), 23= (Strussman and Carvalho 2001), 24= (Hoogmoed & Ávila-Pires, 1991), 25= (Duméril and Bibron 1839), 26= (Teixeira et al. 2014), 27= (Gonzalez-Sponga and Gans 1971), 28= (Señaris 1999), 29= (Gans 1971), 30= (Gans and Mathers 1977), 31= (Vanzolini 1991c), 32= (Schmidt 1936), 33= (Vanzolini 1950), 34= (Rodrigues et al. 2003), 35= (Rojas et al. 2016), 36= (Costa et al. 2018b), 37= (Vanzolini 1996), 38= (Meza-Joya 2015), 39= (Klappenbach 1960), 40= (Hoogmoed 1989), 41= (Gans 1966), 42= (Souza e Lima et al. 2014), 43= (Cope 1875), 44= (Noble 1921), 45= (Gray 1872), 46= (Werner 1901), 47= (Cope 1885), 48= (Boulenger 1890), 49= (Lancini 1963), 50= (Costa et al. 2018a), 51= (Vanzolini 1994), 52= (Castro-Mello 2003), 53= (Boulenger 1907), 54= (Gans 1967), 55= (Thomas 1966), 56= (Boulenger 1915), 57= (Strauch 1881), 58 = (Ruthven 1922), 59= (Mott et al. 2009), 60= (Vanzolini 1995), 61= (Costa et al. 2019), 62= (Stejneger 1911), 63= (Ruiz-García et al. 2016), 64= (Vanzolini 1971), 65= (Wagler 1824).

Sex determinations were performed by direct dissections. Furthermore, we made measurements of the head scales on fixed specimens, taking digital pictures using a Zeiss Axiocam microscope camera installed on a stereo microscope Carl Zeiss model stemi 2000c and the software Image-J version 1.52 (Schneider et al. 2012). We measured the following morphometric characters: head length (HL); head width (HW); prefrontal length (PFL); prefrontal width (PFW); frontal length (FL); frontal width (FW); parietal length (PL); parietal width (PW); ocular length (OL); ocular height (OH); postocular length (POL); postocular width (POW); first temporal length (TEL); first temporal height (TEH); mental length (ML); mental width (MW); post mental length (PML); post mental width (PMW). Additionally, we took the following body size measurements using a measuring tape (±1 mm): snout-vent length (SVL) and caudal length (TL). We also took body diameter (BD) at mid-body using a digital caliper (±0.01 mm).

Results

Phylogenetic analyses and genetic divergence

The tree-building methods revealed Amphisbaena elbakyanae sp. nov. with robust support (BA: 0.91) as a sister taxon of a highly supported clade (BA: 0.97), comprising a specimen of A. cunhai Hoogmoed & Ávila-Pires, 1991 FJ441916 and specimens of A. mertensii Strauch, 1881 FJ441917, FJ441919, and FJ44191 (Fig. 1). Furthermore, A. elbakyanae sp. nov. appeared evolutionarily distant from sequences belonging to individuals from the sympatric species A. fuliginosa and A. alba (Fig. 1). The uncorrected p distances for the ND2 gene showed that the sequence differentiation values between Amphisbaena elbakyanae sp. nov. versus A. cunhai and A. mertensii were 28.9 % and 26.1%, respectively. Furthermore, sequence differentiation values between the new species versus the individuals of the sympatric species A. alba and A. fuliginosa were 26.2% and 28.4%, respectively. The sequence divergence ranges of A. elbakyanae sp. nov. compared to other Antillean and South American taxa was 23.5–30.8% (Table 3).

Figure 1. 

Bayesian inference tree showing the evolutionary relationships of Amphisbaena elbakyanae sp. nov. (red) based on 1029 bp of mitochondrial DNA. Numbers before nodes: posterior probability values. Asterisks indicate maximum support.

Table 3.
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Uncorrected p distances for the fragment of ND2 gene (763 bp) of the species of Amphisbaena expressed as percentages (averages). Values below the diagonal represent between lineage divergences. Bold values along the diagonal depict within lineage divergence.

Species n elb alb ful ane anu ano are bah bol bra cae cam car cai cui cun dar has ign kin kra lee leu mer mit mun pre rob sax sil sch uro ven
A. elbakyanae sp. nov. 1 ―
A. alba 11 26.2 7.2
A. fuliginosa 5 28.4 28.1 7.1
A. anaemariae 1 27.5 27.1 29.3 ―
A. angustifrons 1 28.1 25.7 29.1 24.8 ―
A. anomala 2 28.7 26.6 30.1 29.2 26.2 0.0
A. arenaria 1 27.0 19.4 27.1 26.5 25.1 26.8 ―
A. bahiana 2 30.8 30.0 30.9 29.9 29.5 28.6 30.2 0.2
A. bolivica 2 27.0 18.1 29.9 28.3 27.3 28.3 21.0 28.3 5.8
A. brasiliana 1 25.4 25.7 26.5 27.8 26.8 24.8 24.2 29.5 27.8 ―
A. caeca 1 27.8 26.9 29.8 27.3 24.2 24.6 26.1 28.5 27.7 27.6 ―
A. camura 1 28.7 19.1 30.1 29.7 28.7 27.9 21.8 29.1 6.8 27.9 28.7 ―
A. carli 1 23.5 17.7 27.0 26.6 22.4 23.9 12.8 28.8 18.4 21.8 22.6 19.5 ―
A. cf. caiari 2 29.2 28.6 29.1 29.8 27.4 31.9 28.2 30.7 27.3 28.1 28.8 28.1 25.2 1.7
A. cuiabana 2 25.8 26.4 28.4 26.0 26.3 26.8 26.2 26.5 26.8 24.9 24.5 28.7 23.0 28.3 18.1
A. cunhai 1 28.9 30.4 30.3 32.8 30.9 32.8 30.3 32.7 30.1 30.3 31.2 29.8 27.0 31.3 30.4 ―
A. darwini 1 28.6 24.0 29.8 24.5 18.5 26.4 26.5 27.8 27.6 27.8 23.5 28.6 23.5 27.6 24.8 31.6 ―
A. hastata 2 32.7 32.7 30.8 33.4 31.1 32.3 30.9 29.8 32.3 30.8 31.2 33.1 28.7 30.8 27.2 32.8 29.7 0.0
A. ignatiana 2 26.5 19.4 29.0 27.8 27.0 27.9 16.3 27.6 21.6 24.2 27.2 21.8 15.3 27.5 26.1 27.5 27.6 30.5 0.0
A. kingii 2 27.5 24.7 29.6 23.7 17.3 25.4 25.0 28.3 26.1 24.6 23.1 27.9 21.6 27.9 24.2 30.6 16.8 29.8 27.2 0.0
A. kraoh 1 25.1 19.8 28.8 27.0 25.9 25.4 14.6 29.1 22.0 25.4 25.3 21.7 13.2 28.7 25.9 28.3 25.7 30.5 19.3 24.6 ―
A. leeseri 1 28.7 27.2 29.4 27.0 19.2 25.1 26.4 29.0 28.0 26.5 25.3 29.4 25.2 28.2 25.6 33.0 20.6 30.8 28.4 18.7 25.9 ―
A. leucocephala 2 28.2 18.0 27.8 28.6 28.0 26.5 20.6 29.5 18.9 26.5 27.0 19.3 19.3 27.9 26.3 31.4 26.9 31.8 21.4 25.0 21.4 28.4 6.1
A. mertensii 3 26.1 26.5 30.2 30.7 27.3 28.0 26.9 29.3 27.1 27.6 28.4 27.2 23.6 29.9 28.0 25.0 28.0 32.9 24.6 27.0 26.8 29.4 26.4 11.4
A. mitchelli 1 27.5 26.9 31.2 30.3 27.6 30.0 29.7 31.2 26.8 27.2 28.6 27.9 25.6 27.3 27.3 32.0 27.2 30.3 26.5 27.5 27.2 27.6 26.0 28.0 ―
A. munoai 1 29.8 25.0 29.7 27.5 19.0 25.7 25.9 27.7 28.1 28.9 24.6 28.9 24.5 30.3 25.5 31.9 11.1 30.5 27.9 17.9 26.7 20.7 26.9 29.3 28.1 ―
A. pretrei 2 26.5 16.4 27.3 27.5 28.0 25.9 19.7 29.4 19.1 27.1 25.8 20.2 17.1 28.9 27.6 28.3 26.7 31.2 19.4 26.4 18.9 28.3 16.9 27.0 27.8 27.2 0.0
A. roberti 2 27.9 22.1 29.1 28.6 27.0 28.3 22.5 30.1 23.0 25.9 28.0 24.1 22.0 24.0 26.6 30.5 26.3 31.9 21.9 25.9 22.9 27.9 21.9 27.1 25.5 27.2 21.8 28.3
A. saxosa 2 25.6 19.2 27.2 25.7 22.9 25.0 14.1 28.1 20.3 23.4 22.4 20.7 8.4 26.5 24.6 29.0 25.1 29.2 16.0 21.8 13.3 23.7 20.2 25.1 27.5 23.9 18.2 21.6 0.0
A. silvestrii 2 27.6 25.5 28.3 19.4 23.7 27.2 23.8 27.7 26.5 27.6 25.8 26.8 22.0 27.2 25.3 31.6 22.7 28.9 25.1 24.3 23.8 24.4 27.9 28.5 27.8 23.9 27.9 26.5 21.6 0.8
A. schmidti 3 27.2 26.8 29.0 27.6 26.1 27.2 25.0 27.2 26.8 26.4 23.7 28.1 22.2 29.7 24.6 29.8 25.9 29.8 25.6 22.9 24.6 25.3 25.9 26.7 27.8 26.1 26.6 26.3 22.9 25.1 0.0
A. uroxena 2 30.3 29.0 32.8 29.4 28.5 28.5 29.4 25.0 29.4 29.3 28.7 29.5 26.8 31.5 27.8 33.1 27.4 32.9 27.2 26.9 27.9 27.9 28.9 29.9 31.4 28.3 28.3 30.1 27.0 26.6 27.7 0.5
A. ventrimacularis 6 27.1 16.1 27.4 26.9 26.3 27.2 17.7 29.8 18.8 25.2 27.4 19.9 17.2 27.2 24.5 30.5 25.2 31.6 16.9 25.0 19.7 27.0 18.2 25.2 26.7 26.6 18.2 16.3 18.3 24.6 24.8 28.3 0.5
A. xera 1 29.8 26.3 29.6 27.5 25.6 25.6 25.4 27.0 28.2 25.6 19.6 29.4 23.9 28.2 25.5 32.3 25.6 30.9 25.1 24.6 26.1 25.3 26.8 26.8 28.6 24.2 28.1 26.8 22.8 26.1 23.5 27.9 25.8

New species description

Amphisbaena elbakyanae sp. nov.

http://zoobank.org/5E06051E-F7CC-4C62-8DCB-057389584A65
Figs 2, 3, 4.

Chresonymy: Amphisbaena sp. (ICN-TAS 700): Pedroza-Banda et al. (2014).

Holotype

(Fig. 2). Specimen MLS 1901, a male from El Porvenir farm, Vereda La Colombina, municipality of Paz de Ariporo, department of Casanare, Colombia. Coordinates: N 6.043472222, W –71.09283333; elevation 140 m. a.s.l. The specimen was collected by Teddy Angarita-Sierra, Marvin Anganoy-Criollo and John Jairo Ospina-Sarria, on 20th August 2012, in a riparian forest near the Ariporo River, under leaf litter of the moriche palm (Mauritia flexuosa). This specimen was found in sympatry with A. alba.

Figure 2. 

Holotype Amphisbaena elbakyanae sp. nov. in preservation (MLS 1901, male). (A) Doral view of the head; (B) Lateral view of the head; (C) Ventral view of the head; (D) Ventral view of the tail (tail is autotomized).

Paratypes

Two specimens: MUJ 806, a female from Bojonawi Natural Reserve, Fundación Omacha, municipality of Puerto Carreño, department of Vichada, Colombia. Coordinates: N 6.097997222, W –67.48321667; elevation 54 m a.s.l., collected by Melissa Cuevas in July 2005. MLS 1902, a female from Caño El Socorro, between veredas Aguaverde and La Virgen, municipality of Orocué, department of Casanare, Colombia. Coordinates: N 5.02901, W –71.18037; elevation 128 m. a.s.l., collected by Marvin Anganoy-Criollo in December 2012, under a pile of palm leaves of moriche palm.

Generic placement

Amphisbaena elbakyanae sp. nov. belong to the genus Amphisbaena Linnaeus, 1758 (sensu Mertens 1925; Vanzolini 1951; Gans and Alexander 1962) by having the following characters: (1) Snout rounded, flattened or slightly convexed above; (2) upper head scales paired; (3) rostral scale short, subtriangular, ventrally expanded and posteriorly without contact with prefrontal scales; (4) nasal scales in broad contact; (5) six premaxillary teeth; (6) ten maxillary teeth.

Diagnosis

Amphisbaena elbakyanae sp. nov., can be distinguished from all its congeners by the following combination of characters: (1) three supralabial scales; (2) three infralabial scales; (3) second supralabial scale longer than first and third supralabial scales, contacting first and third supralabial, temporal, ocular and prefrontal scales; (4) angulus oris lies in transverse plane passing through the posterior edges of the ocular scales and the center of the frontal scales; (5) second infralabial scale in contact with postmental scales; (6) six premaxillar teeth; (7) ten maxillar teeth; (8) one temporal scale; (9) absence of malar scale; (10) a single postgenial scale row with four segments; (11) postmalar scale rows with six to seven segments; (12) first body annulus includes one large segment on each side lying immediately posterior to inner parietal scales, abutting onto posterolateral edge of the outer parietal scales; (13) middorsal segments of second and third body annulus non-enlarged; (14) 245–257 body annuli; (15) 13–15 dorsal segments per annulus at midbody; (16) 16–18 ventral segments per annulus at midbody; (17) four precloacal pores; (18) autotomy sites located on sixth to eighth caudal annuli, (19) 20–24 caudal annuli, (20) rostral scale visible from above, (21) dorsal and ventral surfaces homogeneusly dark brown or dark brown-reddish, (22), and small body size 211–237 mm (Fig. 3).

Figure 3. 

Comparison of the head scuttelation between the holotypes of Amphisbaena elbakyanae sp. nov. and A. gracilis. (A, C, E) Dorsal, lateral and ventral view of the head of A. elbakyanae sp. nov. (B, D, F) Dorsal, lateral and ventral view of the head of A. gracilis. (G) Lateral view of the caudal scuttelation of A. elbakyanae sp. nov. Scales: 1 = nasals, 2 = prefrontals, 3 = frontals, 4 = oculars, 5 = rostral, 6 = supralabials, 7 = posoclulars, 8 = temporals, 9 = parietals, 10 = middorsals segments of the body annulus, 11 = first, second and third body annulus, 12 = infralabials, 13 = mental, 14 = postmentals, 15 = postgenials, 16 = postmalars, 17 = precloacal annulus, 18 = cloacal annuli, 19 = postcloacal annulus, 20 = autotomus annulus, 21 = postclocal lip, 22 = precloacal lip.

Comparisons

(Table 2). Among all four-pored Amphisbaena species from South American, Amphisbaena cunhai, A. frontalis, A. gracilis, A. medemi, A. talisiae and A. slateri are the most similar species. Nonetheless, A. elbakyanae sp. nov. can be distinguished by having 245–257 body annuli (versus 226–239 in A. cunhai, 252–272 in A. frontalis, 224–248 in A. gracilis, 230–235 in A. medemi, 205–234 in A. talisiae, and 176–213 in A. slateri); 20–24 caudal annuli (versus 25–26 A. cunhai, 17–18 in A. medemi); a single postgenial scale row composed by four segments (versus two postgenial scale rows in A. medemi and A. slateri); absence of malar scales (versus a single malar scale in A. cunhai, A. slateri and A. talisiae); postmalar scale row composed by six to seven segments (versus nine segments in A. medemi); rostral scale visible from above (versus rostral scale non-visible from above in A. gracilis. Fig. 3A–B), first body annulus includes one large segment on each side lying immediately posterior to inner parietal scales, abutting onto posterolateral edge of the outer-parietal scales (versus first body annulus including two or three, large segments on each side lying immediately posterior to inner parietal scales, abutting onto posterolateral edge of the outer parietal scales in A. gracilis, Fig. 3A–B); middorsal segments of second and third body annuli non-enlarged (versus three or four middorsal segments of second and third body annuli enlarged in A. gracilis, Fig. 3A–B) and angulus oris lies in transverse plane that passes through posterior edges of the ocular scales and center of frontal scales [versus angulus oris lies in transverse plane that passes through posterior edges of the postocular scales and center of parietal scales in A. gracilis, Fig. 3E–F (Gonzalez-Sponga and Gans 1971)]. Additionally, Amphisbaena elbakyanae sp. nov. can be distinguished from A. mertensii (one of phylogenetically closely related species, Fig. 1) by having four pre-cloacal pores and 245–257 body annuli (versus 6–8 and 210–250 in A. mertensii, respectively). Comparisons with the remaining four-pored Amphisbaena species are summarized in Table 2.

Description of holotype

(Figs 2–4; Table 4). Male, small body size (SVL = 211 mm; TL = Incomplete tail); slender body (BD = 5.3 mm); head and body slightly differentiated by a small nuchal constriction; head longer than wide (HW/HL 77.7%); snout rounded; six premaxillary teeth beginning with two large, anteromedian teeth that are flanked on either side by a posteriorly directed row of two slightly recurved teeth that gradually diminish in size; ten maxillary slightly recurved teeth that gradually diminish in size arrayed in an oblique row; rostral scale visible from above, subtriangular, ventrally expanded, wider and concave posteriorly, narrowly contacting first supralabial and broadly contacting with nasal scales; nasal, prefrontal, frontal and parietal scales from both sides contacting along the midline of the head forming a longitudinal suture (Figs 2A, 3A); nasal scale quadrangular, contacting the first supralabial, prefrontal and rostral scales; nostrils lateral in the anteroventral part of nasal scale; prefrontal scales roughly pentagonal, wider than long (PFW/PFL 92.9%), broadly contacting nasal, frontal, ocular, first and second supralabial scales, having a narrow contact with first supralabial scale and a broad contact with second supralabial scale (Figs 2A, 3A); frontal scales trapezoidal, longer than wide (FW/FL 63.0%), in broad contact with prefrontal, postocular and inner parietal scales and in narrow contact with ocular scale. Four parietal scales roughly pentagonal; inner parietal scales longer than wide (IPW/IPL 91.4%), in broad contact with frontal, postocular, and outer-parietal scales, as well as with the middorsal enlarged segments of the first body annulus; outer parietal scales wider than long (OPL/OPW 91.8%) , in broad contact with inner-parietal and postocular scales; first body annular non-enlarged scales, but in narrow contact with middorsal enlarged segments of the first body annulus; angulus oris lies in transverse plane that passes through posterior edges of the ocular scales and center of frontal scales (Figs 2B, 3E); three supralabial scales, first subtriangular, longer than wide in broad contact with nasal and second supralabial scales, in narrow contact with prefrontal and rostral scales; the second supralabial larger than the first one and third supralabial scales, contacting first and third supralabial, temporal, ocular and prefrontal scales; third supralabial scale smaller than first and second supralabial scales, contacting second supralabial, temporal and in posterior contact with first body annulus; ocular scales rhomboidal, longer than high (OH/OL 62.4%), in broad contact with prefrontal, postocular, temporal and second supralabial scales, in narrow contact with frontal scales; eye slightly visible in the anterior corner of the ocular scale; postocular scales roughly hexagonal, longer than wide (POW/POL 84.8%), broadly contacting frontal, parietal, ocular, temporal and in posterior contact with first body annulus; one temporal scale roughly pentagonal longer than wide (THE/TEL 68.1%) broadly contacting second and third supralabial and ocular scales, as well as the first body annular scales.

Table 4.
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Measurements (in mm) of holotype and paratype series of Amphisbaena elbakyanae sp. nov.

Trait (mm) MLS 1901* MLS 1902 MUJ 806
Sex Male Female Female
SVL 211 237 224
TL incomplete 27 20
BD 5.3 5.6 5.9
HL 7.1 7.0 6.4
HW 5.5 5.3 5.2
PFL 1.9 2.2 2.5
PFW 1.8 1.7 1.4
FL 1.8 2.0 1.8
FW 1.1 1.2 1.1
IPL 1.4 1.5 1.6
IPW 1.3 1.3 1.3
OPL 1.2 1.2 1.5
OPW 1.3 1.3 1.4
OL 1.6 1.3 1.2
OH 1.0 0.9 0.9
POL 1.4 1.6 1.6
POW 1.2 1.0 0.8
TEL 1.6 1.3 1.4
TEH 1.1 1.2 1.2
ML 1.2 1.4 1.3
MW 1.1 1.2 1.1
PML 2.0 1.9 1.9
PMW 1.4 1.4 1.5

Snout ventral length (SVL), caudal length (TL), head length (HL), head width (HW), prefrontal length (PFL), prefrontal width (PFW), frontal length (FL), frontal width (FW), inner parietal scales length (IPL), inner parietal scales width (IPW), outer parietal scales length (OPL), outer parietal scales width (OPW), ocular length (OL), ocular height (OH), postocular length (POL), postocular width (POW), first temporal length (TEL), first temporal height (TEH), mental length (ML), mental width (MW), postmental length (PML), postmental width (PMW). Asterisk (*) indicates the holotype.

Mental scales quadrate, smaller and narrower than rostral scale, longer than wide (MW/ML 94.8%), in broad contact with postmental and first infralabial scales; postmental scale oblong, longer than wide (PMW/PML 70.3%), visible longer than and in broad contact with mental scale, first and second infralabials and postgenial scale row; three infralabial scales, first trapezoidal, longer than wide and in broad contact with mental, postmental and second supralabial scales; second infralabial scale larger than first and third infralabial scales, broadly contacting first and third infralabial and postmalar scale rows; third infralabial scale smaller than first and second infralabial scales, in contact with second infralabial scale, postmalar scale row and in posterior contact with first body annulus; malar scales absent; postgenial scale row composed by four segments, in contact with second infralabial, postmental, and in posterior contact with postmalar row of scales; postmalar row of scales composed by seven segments (Figs 2C, 3C).

Body annuli demarcated; lateral and middorsal sulci present, beginning from 16th (left) or 18th (right) body annulus; 245 body annuli, 13 dorsal segments per annulus at midbody, 16 ventral segments per annulus at midbody; first body annulus with one enlarged middorsal segment on each side contacting with posterior edge of the inner parietals, abutting onto posterolateral edge of the outer parietal scales; middorsal segments of second and third body annulus non-enlarged (Figs 2A, 3A); four precloacal pores rounded; anal flap semicircular; four cloacal annuli, six caudal annuli (incomplete tail), caudal autotomy site between sixth to seventh caudal annuli (Figs 2D, 3G).

Color of the holotype in life (Fig. 4). Dorsal and ventral surfaces from dark brown to dark brown-reddish; occipital, parietal, frontal, temporal, third supralabial, third infralabial, postmental scales, as well as postgenial and postmalar scale rows dark brown highly pigmented; rostral, prefrontal, ocular, nasal, first and second supralabial, mental and first infralabial scales dark brown faded.

Figure 4. 

Color in life of Amphisbaena elbakyanae sp. nov. (A) Holotype of A. elbakyanae sp. nov., recently euthanized (MLS 1901, male). (B) Specimen in life of A. elbakyanae sp. nov. from paratype locality: Bojonawi Natural Reserve, Fundación Omacha, municipality of Puerto Carreño, Vichada Department, Colombia (N 6.097997222, W - 67.48321667; elevation 54 m. a.s.l.). Photo by Beiker Castañeda.

Color of the holotype in preservative

(Fig. 2). After seven years in preservative, dorsal and ventral surfaces, as well as head scales maintained dark brown coloration having slight differences with color in life, such as a faint grey coloration on dorsal and ventral surfaces, and a few unpigmented scales.

Etymology

We dedicate this species to the Kazakhstani scientist Alexandra Asanovna Elbakyan (Russian: Алекса́ндра Аса́новна Элбакя́н), creator of the web site Sci-Hub, for her colossal contributions for reducing the barriers in the way of science, as well as her reclamation that “everyone has the right to participate and share in scientific advancement and its benefits, freely and without economic constraints”.

Distribution and natural history

The known localities of Amphisbaena elbakyanae sp. nov., are distributed in the flooded savanna ecosystem of the Orocué and Ariporo River basin, as well as in the drained savanna ecosystem of the Bita River basin in the department of Vichada (Fig. 5). Amphisbaena elbakyanae sp. nov. seems to be highly associated with the leaf litter of the savanna flood forest dominated by moriche palm (Mauritia flexuosa), which are commonly known as “morichales” or “cananguchales” in Colombia (Fig. 6). The new species was found in sympatry with A. alba and A. fuliginosa.

Figure 5. 

Geographic distribution of Amphisbaena elbakyanae sp. nov. detailing the soil type where each specimen was collected. The black star represents the holotype locality. The black triangles represent the localities of the paratypes. Background map was retrieved from the Esri open database accessing the following sources: DeLorme, USDS, NPS; USGS, NOAA.

Figure 6. 

Habitat of Amphisbaena elbakyanae sp. nov. (A) Panoramic view of savanna flood forest dominated by moriche palm at the Bita River, Department of Vichada, Colombia. (B) Microhabitats inside of moriche palm’s forest. (C) Moriche palm (Mauritia flexuosa).

Discussion

In this research, molecular and morphological evidence allowed us to confirm that Amphisbaena elbakyanae sp. nov. represents a new species of amphisbaenian from northern South America (sensu Eva and Huber 2005). Our phylogenetic analysis suggests that Amphisbaena elbakyanae sp. nov. together with A. cunhai and A. mertensii from central-southern Brazil, is part of the same monophyletic clade (Fig. 1). However, great genetic distances for the ND2 gene fragment were revealed between Amphisbaena elbakyanae sp. nov. versus A. cunhai and A. mertensii (28.9% and 26.1%, respectively). Currently, molecular data of several species from northern South America is lacking (e.g. A. medemi, A. spurrelli, A. gracilis, A. vanzolinii, and A. steinegeri), limiting the understanding of the evolutionary relations of northern-South American amphisbaenians. Therefore, it is crucial to include many more taxa, to formulate a complete phylogenetic hypothesis that may reduce spurious phylogenetic relationships, basal polytomies and poorly supported nodes (Teixeira et al. 2014). Despite the scarcity of the molecular data, our analyses revealed that the new taxon is not closely related to the sympatric species A. alba or A. fuliginosa (Fig. 1), confirmed by the great genetic distances between them (Table 3). The morphological evidence analyzed allowed us to clearly diagnose Amphisbaena elbakyanae sp. nov. as a different lineage compared to the 50 nominal four pored Amphisbaena species, demonstrating that it was an undescribed species of worm lizard from Colombia.

Furthermore, both molecular and morphological evidence agreed with Gans and Mathers (1977) group’s division of the amphisbaenians from northern South America: The first group included two larger and wide-ranging species (A. alba and A. fuliginosa), and the second group comprised six smaller narrow-ranging species (A. gracilis, A. medemi, A. rozei, A. spurrelli, A. stejnegeri and A. vanzolinii). Based on the morphological characters of Amphisbaena elbakyanae sp. nov., this taxon can be allocated into Gans and Mathersʼ second group. Interestingly, Amphisbaena elbakyanae sp. nov., exhibited a close morphological similarity with both closely distributed taxon (e.g. A. gracilis) and geographically distant taxa (e.g. A. cunhai, A. frontalis, A. talisiae and A. slateri) . Moreover, Amphisbaena elbakyanae sp. nov. and A. gracilis are the continental worm lizards that seem to have the greatest affinity with the Antillean Amphisbaena species by showing a lack of malar scales, four precloacal pores, relatively small size and uniform dorsal and ventral pigmentation. Aditionally, A. elbakyanae sp. nov. together with A. gracilis and A. medemi are the only forms of the northern mainland that have fewer dorsal rather than ventral segments to a midbody annulus closely resembling the Antillean Amphisbaena species (Gans and Alexander 1962; Gonzalez and Gans 1971; Gans and Mathers 1977).

This situation leaves open the question of whether such morphological similarities are due to evolutionary ancestry or could be due to convergent evolution of characters, a product of adaptation to similar habitats (Harmon et al. 2005; Edwards et al. 2012). Some authors have claimed that parallelism, understood as the independent evolution of similar traits, starting from a similar ancestral condition, could be another possibility for morphological similarities between Amphisbaena species (Mott and Vieites 2009). Vidal et al. (2008) dated the split between African and South American Amphisbaenidae at 40 Mya ago (Eocene), proposing that transatlantic dispersal from Africa to South America + West Indies could explain this divergence. According to Gonzalez and Gans (1971), the West Indies species may be the ancestors of the northern South American Amphisbaena species. Consequently, the similarities between some Antillean and South American species may have resulted from the retention of a primitive character pattern in a zone geographically peripheral to the range of the genus. Although we cannot assess directly Gonzalez-Sponga and Gan’s hypothesis, the distant evolutionary relationship between Amphisbaena elbakyanae sp. nov. and the Antillean species A. caeca and A. xera revealed by our phylogenetic and genetic distance analyses (Fig. 1; Table 3), as well as the distant relationships showed by Pyron et al. (2013; fig. 12K) between A. cunhai and A. mertensii (species that form a monophyletic clade together with Amphisbaena elbakyanae sp. nov.) and the Antillean species (i.e. A. bakeri, A. caeca, A. cubana, A. fenestrate, A. manni, A. schmidti and A. xera), suggest that recent evolutionary ancestry may not be the cause of the morphological similarities. Those and many more questions concerning northern South American worm lizards remain open, evidence that the state of knowledge for many fields is still extremely fragmentary.

Conclusions

Amphisbaena elbakyanae sp. nov., described as a new species from the Orinoquia savanna ecosystem of Colombia, seems to be related to A. cunhai and A. mertensii from central-southern Brazil. This species of Amphisbaena is one of the several still-unrecognized evolutionary lineages of worm lizards that are deposed in Colombian museum shelves waiting to be described. We think that the lack of worm lizard studies in Colombia is derived from three main factors. First, insufficient funding for field and museum research; second, large areas still lack intensive sampling and third, there are few investigators searching for worm lizards and few experts and trained personnel capable of describing species (Gascon et al. 2007; Ospina-Sarria and Angarita-Sierra 2020). Therefore, the description of this new Amphisbaena species points out the urgent need to generate a research grant program that could support field surveys and research on several disciplines to increase our knowledge of worm lizards, as well as help to train researchers to describe species including the known but yet-undescribed species currently housed in Colombian biological collections. Studies of taxonomy and species descriptions in a megadiverse country like Colombia play a substantial role in the conservation of our natural heritage. Thus, encouraging these activities will allow an evaluation of biodiversity loss and the development of systematic conservation planning and practices, as well as a scientific focus on value judgments that make up environmental policies and laws.

Key to the Colombian worm lizard species

(1) Snout prognathous; rostral scale large, elongate and coniform in broad contact with prefrontal scales, separating nasal scales (Genus Mesobaena) Mesobaena huebneri
— Snout non-prognathous; rostral scale short, subtriangular, ventrally expanded and posteriorly without contact with prefrontal scales; nasal scales in broad contact (Genus Amphisbaena) 2
(2) Robust body; 30–42 dorsal segments per annulus at midbody, 35–46 ventral segments per annulus at midbody, caudal autotomy absent Amphisbaena alba
— Robust or thin body, less than 29 dorsal and ventral segments per annulus at midbody, caudal autotomy present 3
(3) Robust body; 19–28 dorsal segments per annulus at midbody, 21–28 ventral segments per annulus at midbody; 6–9 precloacal pores, postmalar scale row composed by 10–14 segments Amphisbaena fuliginosa
— Thin body, four precloacal pores, postmalar scale row composed by 6–9 segments 4
(4) 245–257 body annuli, 13–15 dorsal segments per annulus at midbody, three supralabial and infralabial scales Amphisbaena elbakyanae sp. nov.
— Less than 244 body annuli 5
(5) 230–235 body annuli, 14–16 dorsal segments per annulus at midbody, three supralabial and infralabial scales Amphisbaena medemi
— 213–222 body annuli, 16–18 dorsal segments per annulus at midbody, four supralabial and infralabial scales Amphisbaena spurrelli

Acknowledgments

We thank John Jairo Ospina-Sarria, Marvin Anganoy-Criollo and Juan Carlos Gómez (Chigüi) for their help and support during the fieldwork. We give special thanks to Esperanza Parales, who hosted us in her farm (El Porvenir) during the fieldwork. We thank Rebeca Morantes-Zamora for her help with the distribution map. We thank Beiker Castañeda, Brayan Marín, Carlos Lasso, as well as Fundación Omacha for provide us a photograph of specimen in life of Amphisbaena elbakyanae from Bojonawi Natural Reserve.We also thank the reserchers of the Biodiversity and Conservation Genetics Group of the Genetics Institute, National University of Colombia for their assistance in the DNA lab. We thank Martha Calderón-Espinosa and John D. Lynch (ICN), Julio Mario Hoyos (MUJ), Andres R. Acosta-Galvis (IAvH), Fernando Sarmiento-Parra and Julieth S. Cardenas-Hincapie (MLS), Juan Manuel Daza (MHUA), Matha Patricia Ramírez and Elson Meneses-Pelayo (UIS) for allowing us to examine specimens of Amphisbaena under their care.

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