New Records and an Updated List of Herpetofauna from Cerro Piedra Larga, an Isolated Mountain Massif in Oaxaca, Mexico

Home , Craugastor pygmaeus, Crotalus ravus, Enulius, Lepidophyma smithii, Leptophis diplotropis, Plestiodon brevirostris

Herpetology Notes, volume 10: 651-658 (2017) (published online on 23 November 2017)

New records and an updated list of herpetofauna from Cerro Piedra Larga, an isolated mountain massif in Oaxaca, Mexico

Rafael Alejandro Calzada-Arciniega1,*, Ernesto Recuero2, 3, Mirna G. García-Castillo1 and Gabriela Parra-Olea1

Abstract. Oaxaca has the highest diversity of amphibians and reptiles of all the states in Mexico. �� mountain located in the southeast region of Oaxaca; �� by drier lowlands. A previous study reported a high diversity of vertebrate fauna on the massif, with 34 species of herpetofauna. During a sampling field trip to Cerro Piedra Larga in September 2014 we found a total of 22 species of amphibians and reptiles, 10 of which represent new records to the area, including six Mexican endemics. Our new records include two salamander species known previously only from their type localities in separate physiographic provinces and the others represent an extension to their geographical known distribution. With the new data we provide herein, Cerro Piedra Larga reaches 42 species of amphibians and reptiles.

Keywords: Amphibians, Reptiles, Conservation, Diversity, Distributional records, Plethodontidae, Salamanders, Checklist

Introduction position in the transition zone between the neartic and neotropical zones (Casas-Andreu et al., 1996). Although The state of Oaxaca in southern Mexico covers an southern Mexico, and specifically the state of Oaxaca, area of 93000 km2 and supports the highest diversity is one of the better studied areas compared to most of of reptiles (293 species) and amphibians (149 species) the northern parts of the country, the known diversity in the country, with very a high degree of endemism of this region increases every year with new records (93 species, 21%). Oaxacan herpetofaunal diversity and new species descriptions, indicating that Oaxacan represents almost 40% of the known amphibians and biodiversity is still underestimated (Mata-Silva et al., reptiles of this megadiverse country (INEGI, 2012; 2015). Here, we provide additional data from one of the Parra-Olea et al., 2014; Flores-Villela and García- areas within Oaxaca: Cerro Piedra Larga, an isolated Vàzquez, 2014; Mata-Silva et al., 2015). The high mountain massif located about 100 km southeast of level of diversity and endemism is primarily due to the Oaxaca city. geological complexity of the state and its geographic

Material and Methods Study area.—Cerro Piedra Larga (also known as 1 Departamento de Zoología, Instituto de Biología, Universidad “Cerro Sacamecate” or “Cerro El Español”) is located Nacional Autónoma de México. City, Mexico. in southeastern Oaxaca, west of the Isthmus of 2 Departamento de Ecología de la Biodiversidad, Instituto de Tehuantepec (Figure 1). Cerro Piedra Larga belongs Ecología, Universidad Nacional Autónoma de México, Ap. to the physiographic province known as Montañas Postal 70-275, Ciudad Universitaria, Mexico City, 04510, y Valles del Centro (MVC) (Ortiz-Pérez et al., 2004). Mexico. Cerro Piedra Larga is of Mesozoic origin and reaches an 3 Departamento de Biodiversidad y Biologia Evolutiva, Museo elevation of 2700 meters above sea level. It is isolated Nacional de Ciencias Naturales, CSIC, c/ José Gutiérrez Abascal, 2, 28006 Madrid, Spain from other montane areas (e. g. Sierra Mixe to the * Corresponding author e-mail: north and Sierra de Miahuatlán to the south) by deep [email protected] dry valleys covered by deciduous tropical scrub forests 652 Rafael Alejandro Calzada-Arciniega et al.

Figure 1. Map showing the location of Cerro Piedra Larga, municipality of San Carlos Yautepec in the state of Oaxaca, México. The mountain is represented by a triangle. �� Bolitoglossa zapoteca at 1 Km E Santa María Ecatepec in Sierra Madre del sur and the type locality of Pseudoeurycea mystax at 0.9 Km E-NE Ayutla in Sierra Mixe.

(Peterson et al., 2004). Due to its isolated position, it m asl. We followed survey methodology as described can be considered biogeographically as a sky island by Casas-Andreu et al. (1991). For each animal found (Warshall, 1994). According to Peterson et al. (2004) we took photographs and field data including the the vegetation in the lower part of the massif is tropical habitat type (e.g. Pine-oak forest, Pine forest, Dry deciduous forest, followed by pine-oak forest between forest, Ecotone between dry forest and pine-oak forest 1800–2200 m asl, and pine forest in the higher area and Cloud forest). For more accurate identification, (2200–2700 m asl). In some areas, usually limited to we collected a few specimens that were fixed in 10% small moist gorges, there are remnants of cloud forest, formalin and preserved in 70% ethanol. Tissues from which is one of the most diverse and threatened habitats collected individuals were preserved in RNAlater® for in Mexico (Ornelas et al., 2013). The only published molecular studies. All collected material is deposited at information on the herpetological community of Cerro the Colección Nacional de Anfibios y Reptiles (CNAR) Piedra Larga came from a preliminary biological survey of the Instituto de Biología, Universidad Nacional recording plants and terrestrial vertebrates, which Autónoma de México (UNAM) in Mexico City included the observation of 34 species of reptiles and (Appendix 1). amphibians (Peterson et al., 2004). Results and Discussion Fieldwork.—Sampling was performed during We found a total of 22 species, including three September 12 – 16 2014. A transect approximately salamanders, seven anurans, nine lizards and three 12 km long was sampled, starting from the village of snakes. Ten of these species represent new records for Asunción Lachixonase, municipality of San Carlos the area, while the other 12 were already reported by Yautepec (16º25’44.8”N, -95º49’33.4”W; 529 m asl), Peterson et al. (2004) (Table 1). This new survey brings and continuing along the dirt road up to a logging camp the known diversity of Cerro Piedra Larga to a total of 42 (N 16º32’5.1”N, 95º48’58.8”W; 1950 m asl). From species. The newly reported species represent the 23.8% there, we performed several shorter transects along of the total of amphibians and reptiles known from the southeast side of the mountain, up to about 2600 Cerro Piedra Larga (Figure 2; Figure 3). Five of the new New records and an updated list of herpetofauna from Cerro Piedra Larga, Mexico 653

Figure 2. Amphibians from Cerro Piedra Larga; A) Incilius canaliferus; B) Incilius occidentalis; C) Rhinella horribilis; D) Exerodonta sumichrasti; E) Eleutherodactylus nitidus; F) Eleutherodactylus pipilans; G) Bolitoglossa zapoteca; H) Pseudoeurycea mystax. 654 Rafael Alejandro Calzada-Arciniega et al.

Figure 3. Reptiles from Cerro Piedra Larga; A) Gerrhonotus liocephalus; B) Sceloporus formosus; C) Sceloporus smithi; D) Scincella gemmingeri; E) Lepidophyma smithii; F) Rhadinaea fulvivittis; G) Leptodeira polysticta; H) Crotalus ravus. New records and an updated list of herpetofauna from Cerro Piedra Larga, Mexico 655

Table 1. Amphibians and reptiles of Cerro Piedra Larga. New records and type of habitat where they have been found [Pine-oak 1 Table 1. Amphibians and reptiles of Cerro Piedra Larga. New records and type of habitat where they have forest (P-O), Pine2 forestbeen (P),found Dry [Pine-oak forest forest (DF), (P-O), Ecotone Pine forestbetween (P), Drydry forestforest (DF), and Ecotone pine-oak between forest dry (E) forest and and cloud pine-oak forest (CF)]. 3 forest (E) and cloud forest (CF)].

New Habitat SPECIES records P-O P DF E CF AMPHIBIA ANURA Bufonidae Incilius canaliferus (Cope, 1877) X Incilius occidentalis (Camerano, 1879) X X Rhinella horribilis (Linnaeus, 1758) X Hylidae Exerodonta sumichrasti Brocchi, 1879 X X Sarcohyla bistincta (Cope, 1877) X Ptychohyla leonhardschultzei (Ahl, 1934) X X Craugastoridae Craugastor pygmaeus (Taylor, 1937) X X Eleutherodactylidae Eleutherodactylus nitidus (Peters, 1870) X X Eleutherodactylus pipilans Taylor, 1940 X CAUDATA Plethodontidae Bolitoglossa zapoteca Parra-Olea et al., 2002 X X X Pseudoeurycea sp. X X X X Pseudoeurycea mystax Bogert, 1967 X X REPTILIA SQUAMATA Anguidae Abronia oaxacae (Günther, 1885) X Gerrhonotus liocephalus Wiegmann, 1828 X X Eublepharidae Coleonyx elegans Gray, 1845 X Gekkonidae Hemidactylus frenatus Duméril & Bibron, 1836 X X Dactyloidae Anolis sacamecatensis Köhler et al, 2014 X Iguanidae Ctenosaura oaxacana Köhler & Hasbún, 2001 Phrynosomatidae Sceloporus formosus Wiegmann, 1834 X X Sceloporus grammicus Wiegmann, 1828 X Sceloporus siniferus Cope, 1869 X X Sceloporus smithi Hartweg & Oliver, 1937 X X 1 Urosaurus bicarinatus (Duméril, 1856) X Phyllodactylidae Phyllodactylus muralis Taylor, 1940 X Scincidae Plestiodon brevirostris (Günther, 1860) X Scincella gemmingeri (Cope, 1864) X X Teiidae Aspidoscelis deppii (Wiegmann, 1834) X Aspidoscelis guttata (Wiegmann, 1834) X Aspidoscelis motaguae Sackett, 1941 X Xantusiidae Lepidophyma smithii Bocourt, 1876 X X Dipsadidae Rhadinaea fulvivittis Cope, 1875 X Leptodeira polysticta (Günther, 1885) X X Colubridae Senticolis triaspis (Cope, 1866) X Enulius flavitorques (Cope, 1868) X Leptophis diplotropis (Günther, 1872) X X Tantilla striata Dunn, 1928 X Trimorphodon biscutatus (Duméril et al., 1854) X Natricidae Thamnophis lineri Rossman & Burbrink, 2005 X Leptotyphlopidae Epictia schneideri Wallach, 2016 X Elapidae Micrurus ephippifer (Cope, 1886) X Viperidae Crotalus ravus Cope, 1865 X Bataguridae Rhynoclemmys rubida (Cope, 1870) X 4 5 6

2 Sceloporus siniferus Cope, 1869 X X Sceloporus smithi Hartweg & Oliver, 1937 X X Urosaurus bicarinatus (Duméril, 1856) X Phyllodactylidae Phyllodactylus muralis Taylor, 1940 X Scincidae Plestiodon brevirostris (Günther, 1860) X Scincella gemmingeri (Cope, 1864) X X Rafael Alejandro Calzada-Arciniega et al. 656 Teiidae 1 AspidoscelisTable 1. Amphibians deppii (Wiegmann, and reptiles 1834) of Cerro Piedra Larga. New records and type of habitat Xwhere they have Table 1. Continued.2 Aspidoscelisbeen found [Pine-oak guttata (Wiegmann, forest (P-O), 1834) Pine forest (P), Dry forest (DF), Ecotone between dry forestX and pine-oak 3 forest (E) and cloud forest (CF)]. Aspidoscelis motaguae Sackett, 1941 X Xantusiidae New Habitat SPECIES Lepidophyma smithii Bocourt, 1876 records P-O P DFX XE CF AMPHIBIADipsadidae ANURARhadinaea fulvivittis Cope, 1875 X BufonidaeLeptodeira polysticta (Günther, 1885) X X ColubridaeIncilius canaliferus (Cope, 1877) X SenticolisIncilius occidentalis triaspis (Cope, (Camerano, 1866) 1879) X X EnuliusRhinella flavitorques horribilis (Linnaeus, (Cope, 1868) 1758) X HylidaeLeptophis diplotropis (Günther, 1872) X X TantillaExerodonta striata sumichrasti Dunn, 1928 Brocchi, 1879 X X TrimorphodonSarcohyla bistincta biscutatus (Cope, (Duméril 1877) et al., 1854) X X NatricidaePtychohyla leonhardschultzei (Ahl, 1934) X X CraugastoridaeThamnophis lineri Rossman & Burbrink, 2005 X LeptotyphlopidaeCraugastor pygmaeus (Taylor, 1937) X X EleutherodactylidaeEpictia schneideri Wallach, 2016 X ElapidaeEleutherodactylus nitidus (Peters, 1870) X X MicrurusEleutherodactylus ephippifer pipilans (Cope, Taylor, 1886) 1940 X X CAUDATAViperidae PlethodontidaeCrotalus ravus Cope, 1865 X BataguridaeBolitoglossa zapoteca Parra-Olea et al., 2002 X X X RhynoclemmysPseudoeurycea rubidasp. (Cope, 1870) X X X X X 4 Pseudoeurycea mystax Bogert, 1967 X X 5REPTILIA SQUAMATA 6 Anguidae records, Incilius occidentalisAbronia oaxacae, (Günther,Craugastor 1885) pygmaeus, observed juvenileX and adult individuals mainly in pine Gerrhonotus liocephalus Wiegmann, 1828 X X Gerrhonotus liocephalus, Leptodeira polysticta and the forest. Some of these salamanders were found in road Eublepharidae introduced gecko HemidactylusColeonyx elegans frenatus,Gray, 1845 fall within their banks at night as the individualsX collected in the type assumed distributionGekkonidae range (Casas-Andreu et al., 1996; locality by Parra-Olea et al. (2002). However, others 2 Santos-Barrera, 2004;Hemidactylus Santos-Barrera frenatus Duméril and & Bibron, Canseco- 1836 wereX collected under barkX of fallen trees. One Adult Márquez, 2004;Dactyloidae Vázquez-Díaz and Quintero-Díaz, was found active on leaf litter at night after a heavy 2007; Daza et al., Anolis2009; sacamecatensis Martín-Regalado Köhler et al,et 2014al., 2011). rain. PseudoeuryceaX mystax was rarer as we could The records of EleutherodactylusIguanidae nitidus and Scincella only find two adult females in a cloud forest fragment. gemmingeri representCtenosaura the southernmost oaxacana Köhler locality& Hasbún, known2001 Both specimens were found under the leaf litter nearby Phrynosomatidae for the species (Canseco-Márquez, 2007; Santos-Barrera a 1 m diameter rock. We carry out a detailed search Sceloporus formosus Wiegmann, 1834 X X et al., 2010) and alsoSceloporus the first grammicus records Wiegmann, of their 1828 presence in the sameX area but no other salamander was found. in the physiographic province of Montañas y Valles del These observations are especially relevant considering Centro (Mata-Silva et al., 2015). Dixon (1957) showed the conservation status of both species.1 Bolitoglossa a figure representing a locality for E. nitidus near to zapoteca is listed as “data deficient” in the IUCN red ours, but with no further information. list (Parra-Olea et al., 2008) but considered by Mata- Two of our new records correspond to Oaxacan Silva et al. (2015) as “highly vulnerable” according endemic species, the plethodontid salamanders to its Environmental Vulnerability Category (EVC) Bolitoglossa zapoteca and Pseudoeurycea mystax. (Wilson et al., 2013). Pseudoeurycea mystax is listed These species are here reported for the first time outside as “endangered” in the IUCN red list (Parra-Olea and their type localities (Figure 1), located respectively Wake, 2008) and also as “highly vulnerable” according at 1 Km E Santa María Ecatepec, Sierra Madre del to its EVC (Mata-Silva et al., 2015). Sur, Oaxaca (Parra-Olea et al., 2002), and 0.9 Km E- The third salamander found in the area, reported NE Ayutla, Sierra Mixe, Oaxaca (Bogert, 1967). This here as Pseudoeurycea sp., very likely represents an represents a range extension of about 30 Km N-NE for undescribed species which is currently subject of a more B. zapoteca and 60 Km SE for P. mystax (Figure 1). Of detailed study. Peterson et al. (2004) reported a young the two species, B. zapoteca was more common, with 8 specimen of Chiropterotriton sp., deposited in the New records and an updated list of herpetofauna from Cerro Piedra Larga, Mexico 657

Museo de Zoología de la Facultad de Ciencias, UNAM References

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Appendix 1. Voucher specimens. Incilius canaliferus (IBH-29781); Incilius occidentalis (IBH- 30489); Craugastor pygmaeus (IBH-30488, IBH-29777); Eleutherodactylus nitidus (IBH-29776, IBH-29784); Eleutherodactylus pipilans (IBH-29783); Exerodonta sumichrasti (IBH-29785); Bolitoglossa zapoteca (IBH-29780, IBH-29775, IBH-29794, IBH- 29771, IBH-29770, IBH-29774, IBH-29772, IBH- 29778); Pseudoeurycea mystax (IBH-29773, IBH- 29769); Pseudoeurycea sp. (IBH- 29763, IBH-29768, IBH-29762, IBH-29761, IBH-29767, IBH-29765, IBH-29766, IBH-29764); Gerrhonotus liocephalus (IBH-29779); Scincella gemmingeri (IBH-RF-295); Leptodeira polysticta (IBH-30490).

Accepted by Anamarija Zagar