Range extensions of amphibians and reptiles in the southeastern part of the Lacandona rainforest, Mexico

Abstract

The Lacandona rainforest represents one of the most diverse Mexican tropical wet forests. Although some studies have described the amphibians and reptiles of the region, most herpetological lists come from the northern part of the Lacandona, and there are no confirmed records for many of the expected species. We reviewed databases of scientific collections, taxonomy, and published herpetological lists to produce the most recent updated list of amphibian and reptile species in the region (35 amphibians and 90 reptiles). Furthermore, based on recent inventories (2007–2013) we establish 40 range extensions of 8 amphibians and 32 reptiles for the southeastern part of the Lacandona rainforest. Four out of these 40 records confirmed the occurrence of Dermophis mexicanus, Eleutherodactylus leprus, Pantherophis flavirufus, and Bothriechis schlegelii in the region.

Resumen

La selva Lacandona representa uno de los bosques húmedos tropicales más diversos de México. Aunque algunos estudios han descrito a los anfibios y reptiles de la región, la mayoría de los listados herpetológicos proceden de la parte norte de la lacandona y no existen registros confirmados para muchas de las especies esperadas. Se han revisado bases de datos de colecciones científicas, la taxonomía y listados herpetológicos publicados para generar la lista más actualizada de especies de anfibios y reptiles de la región (35 anfibios y 90 reptiles). Además, con base en inventarios recientes (2007–2013) se estableció la extensión del área de distribución de 8 anfibios y 32 reptiles para la parte sureste de la selva Lacandona. Cuatro de estos 40 registros confirmaron la presencia de Dermophis mexicanus, Eleutherodactylus leprus, Pantherophis flavirufus y Bothriechis schlegelii en la región.

Introduction

Mexico is considered the country with the second and fifth highest number of amphibian and reptile species, respectively in the world (Espinosa, Ocegueda, Flores, Llorente-Bousquets, & Vázquez, 2008; Flores-Villela & García-Vázquez, 2014; Parra-Olea, Flores-Villela, & Mendoza-Almeralla, 2014). The Lacandona rainforest contributes greatly to the herpetofaunistic diversity of Mexico and Mesoamerica, being nowadays considered a priority area for biodiversity conservation (Conabio-Conanp-TNC-Pronatura-FCF, UANL, 2007). Yet the available information on species richness and distribution of amphibians and reptiles in the region is incomplete and largely inaccurate (Hernández-Ordóñez et al., 2014).

Hepetofaunal studies in the Lacandona rainforest started in the first half of the 20th century with Smith and Taylor's expeditions (Lee, 1996), and the first published species list for the region reported 77 species, 23 amphibians, and 54 reptiles (Lazcano-Barrero, Gongora-Arones, & Vogt, 1992). After that publication, a number of inventories have reported new records for the region (Ferreira-García & Canseco-Márquez, 2006; Lee, 1996; Muñoz, 2010), including the first Mexican record of the caecilian Gymnopis syntrema (González-Hernández, Hernández-Ordoñez, Cervantes-López, & Reynoso, 2014). New range extensions also have been reported for this rainforest (Paredes-León & Reynoso, 2005a, 2005b, 2005c, 2005d; Percino-Daniel, Barcenas, & Sarabia, 2012; Percino-Daniel, Bénard-Valle, García-del Valle, & Mendelson III, 2013). Nevertheless, in the Lacandona rainforest most studies have been focused on its northern part, and many species have been hypothesized to be present in the region, without any field record that confirms their presence (Köhler, 2011; Lazcano-Barrero et al., 1992).

Here, databases of scientific collections and published herpetological lists that provide a checklist of amphibians and reptiles in the Lacandona rainforest were reviewed. Based on new inventories carried out from 2007 to 2013 in the Marqués de Comillas region, we describe 40 range extensions (8 amphibians and 32 reptiles) for the southeastern Lacandona rainforest. Four out of these 40 records confirmed the occurrence of two amphibian and two reptile species, improving thus the accuracy of the information on the species geographic distributions in the region. We also corrected our previous published species list (Hernández-Ordóñez et al., 2014), by changing Anolis sericeus to Anolis unilobatus, and Marisora unimarginata to Marisora brachypoda, and by excluding Drymarchon corais from this list, as suggested by Crother et al. (2003). Thus, this paper represents the most recent updated list of amphibian and reptile species for the region.

Material and methods

The Lacandona rainforest is located in the southern part of the Mexican state of Chiapas, in southern Mexico (100–1,500 m elev.; Fig. 1). The region has an extension of 13,000 km², bordered to the south and east by Guatemala, and to the east and north by the Mexican state of Tabasco and the Chiapas highlands, respectively; the Palenque National Park represents the northernmost limit of the region (INE, 2000). The Lacandona rainforest is part of the Mayan forest, which represents one of the largest forested areas in Mesoamerica (Rodstrom, Oliviery, & Tangley, 1999). Our study was focused on lowland tropical rainforests (<500 m elev.), dominated by a hot and humid climate, with mean annual precipitation and temperature of 2874 mm and 25 °C, respectively (INE, 2000; Pennington & Sarukhán, 2005).

Figure 1.

Location of previous and new records of amphibians and reptiles in the Lacandona rainforest, Mexico.

To update the checklist of amphibians and reptiles in the Lacandona rainforest, we reviewed all published species lists and range distribution notes from the region (Campbell & Lamar, 2004; Ferreira-García & Canseco-Márquez, 2006; González-Hernández et al., 2014; Lazcano-Barrero et al., 1992; Lee, 1996; Muñoz, 2010; Paredes-León & Reynoso, 2005a, 2005b, 2005c, 2005d; Percino-Daniel et al., 2012, 2013). We consulted databases of the Colección Nacional de Anfibios y Reptiles at the Instituto de Biología (CNAR) and Museo de Zoología at the Facultad de Ciencias (MZFC), both at the Universidad Nacional Autónoma de México (UNAM, Mexico City), the Colección Herpetológica de El Colegio de la Frontera Sur, Unidad San Cristóbal de las Casas (ECOSUR-SC) and the Colección Herpetológica (IHNHERP) of the Secretaría de Medio Ambiente e Historia Natural, both located in Chiapas. Additional data were obtained from the Global Biodiversity Information Facility database, where only records from specimens shelved in scientific collections were considered. We found a specimen of Dermophis mexicanus and a specimen of Coluber mentovarius shelved at CNAR not previously reported for the region. Thus, we confirmed the occurrence of Dermophis mexicanus in the Lacandona rainforest, and extended the distribution range of Coluber mentovarius. Both records are described in Table 1 and Appendix A.

Table 1.

Updated list of amphibian and reptile species in the Lacandona rainforest, Mexico.

Taxa	Previous records^a								Present study^e
	1	2	3	4	5^b	6^c	7^d	8
Class Amphibia
Order Gymnophiona
Family Dermophiidae
Dermophis mexicanus	P					R2			**
Gymnopis syntrema					R3
Order Urodela
Family Plethodontidae
Bolitoglossa mexicana	P	R	R	R		R1	R1,2	R	R
B. mulleri	R		R	R				R	R
B. rufescens	R	P	R	R		R2	R2	R	R*
Oedipina elongata	P			R				R	R*
Order Anura
Family Bufonidae
Incilius campbelli					R2			R	R
I. macrocristatus		R	R						R*
I. valliceps	R	R	R	R		R1,2	R1,2	R	R
Rhinella marina	R	R	R	R		R1	R1	R	R
Family Rhinophrynidae
Rhinophrynus dorsalis	R	P	R	R		R1	R2		R
Family Centrolenidae
Hyalinobatrachium fleischmanni	R		R	R			R2	R	R
Family Hylidae
Agalychnis callidryas	R	R	R	R		R1	R1	R	R
Bromeliohyla bromeliacia		R
Dendropsophus ebraccatus	R	R	R	P		R1	R1,2	R	R
D. microcephalus	R		R	R		R1,2	R1	R	R
Scinax staufferi	P	R	R	R	R1	R1,2	R2	R	R
Smilisca baudinii	R	R	R	R		R1,2	R1,2	R	R
S. cyanosticta	R	R	R	R		R1	R1	R	R*
Tlalocohyla loquax	R		R	R		R2	R1,2	R	R
T. picta	R	P	R	R		R2	R2	R	R
Trachycephalus typhonius	R	R	R	P		R1,2	R2	R	R
Triprion petasatus					R1	R2
Family Microhylidae
Gastrophryne elegans	R		R	P			R2	R	R
Hypopachus variolosus	R
Family Ranidae
Lithobates brownorum		R	R			R1,2	R1,2	R
L. maculatus							R2		R
L. vaillanti	R	P	R	R		R1,2	R1,2	R	R
Family Craugastoridae
Craugastor alfredi	R	R	R	R		R1		R	R*
C. laticeps	R	P		R		R1		R	R*
C. loki		R	R	R		R1	R2	R	R
C. palenque			R			R1		R	R
Family Eleutherodactylidae
Eleutherodactylus leprus	P	P		P					R**
Family Leptodactylidae
Leptodactylus fragilis	R	P	R	R		R1,2	R2	R	R
L. melanonotus	P	P	R	R		R1,2	R2	R	R
Class Reptilia
Order Squamata
Suborder Lacertilia
Family Anguidae
Diploglossus rozellae	R	P		R				R	R*
Family Gekkonidae
Hemidactylus frenatus				R	R1	R1,2		R	R*
Family Sphaerodactylidae
Sphaerodactylus glaucus	R	R		R		R1,2	R1	R	R
S. millepunctatus		P		R				R	R*
Family Phyllodactylidae
Thecadactylus rapicauda	P	R		R		R1	R1	R	R*
Family Eublepharidae
Coleonyx elegans	P	R		R		R1,2		R	R*
Family Polychrotidae
Anolis biporcatus	R	R		R		R1	R1,2	R	R
A. capito	R	R		P		R1	R1	R	R
A. lemurinus	R	R		R		R1,2	R1	R	R
A. pentaprion		R		R		R1		R	R*
A. rodriguezi	R	R		R		R1		R	R
A. tropidonotus	R	P		R		R1	R1,2	R
A. uniformis	R			R		R1,2	R1	R	R*
A. unilobatus	R	R		R		R1,2	R1	R	R
Family Phrynosomatidae
Sceloporus serrifer		R		P	R1	R1,2
S. teapensis		P		R		R1,2		R	R*
Family Iguanidae
Ctenosaura similis				R				R
Iguana iguana	R	R		P		R2	R1		R
Family Corytophanidae
Basiliscus vittatus	R	R		R		R1,2	R1,2	R	R
Corytophanes cristatus	R	R		R		R1		R	R*
Corytophanes hernadezii	R	R		R		R1,2		R
Laemanctus longipes	P			R
Family Scincidae
Marisora brachypoda	P			R				R
Mesoscincus schwartzei		R		P	R2	R1			R
Plestiodon sumichrasti	R	P		R		R2		R	R*
Scincella cherriei	R	R		R		R1	R1,2	R	R
Family Teiidae
Holcosus festivus	P	R		R		R1,2		R	R
Holcosus undulatus	R	R		R		R1	R1,2	R	R
Family Xantusidae
Lepidophyma flavimaculatum	R	R		R		R1,2	R1,2	R	R
Suborder Serpentes
Family Boidae
Boa constrictor	R	P		R		R2	R1,2	R	R
Family Colubridae
Adelphicos quadrivirgatus	P	P		R				R	R*
Amastridium sapperi				R		R2			R*
Clelia clelia	R			P			R1,2		R*
Coluber mentovarius						R2		R	*
Coniophanes bipunctatus	P	P		R				R	R*
C. fissidens	R	P		R				R
C. imperialis	R	P		R			R1	R	R
C. quinquevittatus	R							R
C. schmidti		R		R				R
Drymarchon melanurus	R	R		R				R	R
Drymobius margaritiferus	R	R		R		R1	R1,2	R	R
Ficimia publia				P				R
Geophis carinosus				R
Imantodes cenchoa	R	R		R		R1	R1	R	R
I. gemmistratus	P			R				R
Lampropeltis triangulum	R	P		R				R
Leptodeira frenata	R			R			R1	R
L. septentrionalis	P	R		R		R1,2		R	R*
Leptophis ahaetulla	R	R		R			R1	R	R
L. mexicanus	R	P		R		R2	R1	R	R
Mastigodryas melanolomus	R	P		P				R	R*
Nerodia rhombifer				R		R2
Ninia diademata	P			R				R	R*
N. sebae	P	R		R		R1,2		R	R*
Oxybelis aeneus	P	P		P			R2	R	R*
O. fulgidus	R						R1	R
Oxyrhopus petola	R	R		R		R1	R1,2	R	R
Pliocercus elapoides	P	R		R		R1,2		R	R
Pantherophis flavirufus									R**
Pseustes poecilonotus	R	R		R		R1,2	R1	R	R*
Rhadinaea decorata	R	R		R		R1		R
Scaphiodontophis annulatus	P	R		R		R1			R*
Senticolis triaspis	R			R		R1			R*
Sibon dimidiatus	R	P		R		R1		R	R*
S. nebulatus	R			R		R1	R1	R	R
Spilotes pullatus	R	R		P		R1	R1	R	R*
Stenorrhina degenhardtii	R	P		R			R1	R
Stenorrhina freminvillei				P				R
Tantilla schistosa		R
Tantillita lintoni	P	R		P		R1			R*
Thamnophis marcianus				R
Tretanorhinus nigroluteus	P	R		P		R1			R*
Tropidodipsas sartori		P		R		R2			R*
Xenodon rabdocephalus	R	R		P		R1	R1,2	R	R
Family Elapidae
Micrurus diastema	R	R				R1	R1,2	R	R*
M. elegans	R							R
Family Viperidae
Atropoides mexicanus	P	P		P			R2		R*
Bothriechis schlegelii	P			P		R1			R**
Bothrops asper	R	R		R		R1	R1,2	R	R
Crotalus simus	P			R				R
Porthidium nasutum	R	P		P			R2		R
Order Testudines
Family Emydidae
Trachemys venusta	R	P		R			R1,2	R	R
Family Geomydidae
Rhinoclemmys areolata	P			R
Family Kinosternidae
Kinosternon acutum	R	P		P					R
K. leucostomum	R	P		R			R1	R	R
Staurotypus triporcatus	R	P		R				R
Family Dermatemydidae
Dermatemys mawii	R	R		R		R1,2		R	R
Family Chelydridae
Chelydra serpentina	R	P		R			R1		R
Order Crocodylia
Family Crocodylidae
Crocodylus acutus	R	P		P					R
C. moreletii	R	P		R			R1	R

a

Previous records: 1. Lazcano-Barrero et al. (1992); 2. Ferreira-García and Canseco-Márquez (2006); 3. Muñoz (2010); 4. Lee (1996); 5. New records published between 2005 and 2014; 6. Scientific collections of the Universidad Nacional Autónoma de México (UNAM); 7. Scientific collections in Chiapas state; 8. Online database (Global Biodiversity Information Facility). In all cases, we indicate the species recorded (R) or cited as probable (P) in the region.

b

New records: 1. Paredes-León and Reynoso (2005a, 2005b, 2005c, 2005d); 2. Percino-Daniel et al. (2012, 2013); and 3. González-Hernández et al. (2014).

c

Scientific collections in UNAM: 1. Museo de Zoología de la Facultad de Ciencias (MZFC); 2. Colección Nacional de Anfibios y Reptiles (CNAR).

d

Scientific collections in Chiapas state: 1. Colección Herpetológica Secretaría de Medio Ambiente e Historia Natural (IHNHERP); 2. El Colegio de la Frontera Sur, Unidad San Cristóbal de las Casas (ECOSUR-SC).

e

*Records that represented range extensions for the southeastern part of the Lacandona rainforest (i.e., ≥40 km in straight line from the closest previous records); **records that confirmed the occurrence of certain species in the Lacandona rainforest. In the case of Dermophis mexicanus and Coluber mentovarius, we did not add an ‘R’ in the column for the present study because we have not recorded these species in the region, but we used unpublished records of these species deposited in the Colección Nacional de Anfibios y Reptiles (CNAR).

We also carried out herpetological surveys in the poorly known southeastern part of the Lacandona rainforest, including two adjacent areas separated by the Lacantún River: the Marqués de Comillas region (MCR) and the Montes Azules Biosphere Reserve (MABR), located approximately at 16° 04′ N and 90° 45′ W, and covering an altitudinal range of 100–500 m elev. (Fig. 1). Inventories were conducted during 2007 (February, April, July, September, and November), 2008 (January, March, and July), 2010 (July and October), 2011 (March and August), 2012 (May and June), and 2013 (February) as part of OHO's M.Sc. and Ph.D. thesis (Hernández-Ordóñez, 2009).

Inventories in MCR included old-growth forest patches, secondary forests, crops, bean fields, cocoa plantations, pastures, streams and rivers, human settlements, and roads. We used multiple sampling techniques, including visual encounter surveys, acoustic encounter surveys, drift-fences, pitfalls traps, and boat tours along the Lacantún River (see details of these methods in Corn, 1994; Crump & Scott, 1994; Zimmerman, 1994). Because of the low vagility and the strong philopatry of amphibians and reptiles (Blaustein, Wake, & Sousa, 1994; Böhm et al., 2013; Stuart et al., 2008), the specimens collected ≥40 km in a straight line from the closest previous records were considered as extensions of their geographic range (Canseco-Márquez, Gutiérrez-Mayén, & Salazar-Arenas, 2000; Chrapliwy, 1956; Kraus, 2010).

All specimens were collected under permit No. SGPA/DGVS/02132 of SEMARNAT (Mexican Government) to VHR, and shelved in the Colección Nacional de Anfibios y Reptiles, Instituto de Biología, UNAM. Luis Canseco-Márquez verified most of the specimens. Edmundo Pérez-Ramos verified Adelphicos quadrivirgatus, Joseph Mendelson III verified Incilius macrocristatus, and Alberto Cruz-Silva verified Pantherophis flavirufus.

Results

Our herpetological inventories and detailed revisions of scientific databases revealed a total of 35 species of amphibians from 11 families, and 90 species of reptiles from 22 families for the Lacandona rainforest (Table 1). Within amphibians, anurans had the highest number of species (29 species), followed by salamanders (four species), and caecilians (two species). Regarding reptiles, squamates were the richest with 52 species of snakes and 29 species of lizards, followed by seven species of turtles and two species of crocodiles (Table 1).

We found 40 range extensions for the southeastern part of the Lacandona rainforest (8 amphibians and 32 reptiles; Table 1; Appendix A; Fig. 1). Within these new records, we confirmed the presence of four species (Dermophis mexicanus, Eleutherodactylus leprus, Pantherophis flavirufus, and Bothriechis schlegelii) that had been previously suggested to be present in the region (Table 1).

Discussion

The very high number of species of amphibians and reptiles recorded to date highlights the importance of the Lacandona rainforest to the Mexican herpetofaunistic diversity, as this rainforest represents the second most diverse tropical region in Mexico, just behind the Los Tuxtlas region (Hernández-Ordóñez et al., 2014). Although the Lacandona rainforest covers 0.66% of the Mexican continental territory (about 2,000,000 km²), according to recently published estimates for amphibians (376 species: Parra-Olea et al., 2014; 377 species: González-Hernández et al., 2014) and reptiles (864 species: Flores-Villela & García-Vázquez, 2014), our study indicates that it maintains approximately 9.3% and 10.4% of the amphibian and reptile species in Mexico, respectively. These figures may increase, as there are still some expected species that have not been confirmed for the region. Hernández-Ordóñez et al. (2014) reported 21 species (16 reptiles and 5 amphibians) that have been suggested to be present in the Lacandona rainforest, from which here we confirmed the occurrence of 4 species (2 amphibians and 2 reptiles). Additional studies are therefore needed, particularly in the central and southeastern part of the Marqués de Comillas region (Fig. 1), to have a more accurate herpetofaunal checklist. If the presence of these probable species is confirmed, the Lacandona rainforest will be recognized as the richest rainforest in the country. This information will be essential for biogeographical studies, and will provide a baseline for the ecology and conservation of biodiversity as a whole (Gotelli, 2011; Mace, 2004).

The range extensions between the northern and southern parts of the Lacandona rainforest were relatively expected, as very few surveys have been carried out in the Marqués de Comillas region. In contrast, areas such as the Palenque and Yaxchilán National Parks have been surveyed for decades (Ferreira-García & Canseco-Márquez, 2006; Lee, 1996). Interestingly, range extensions of amphibian species were mainly from Plethodontidae and Craugastoridae, which are known to have restricted distributions (e.g., Oedipina elongata; Campbell, 1998; Lee, 1996). For reptiles, most range extensions were from snakes (Colubridae), that are known to be rare (i.e., with small populations) and/or with low detection probability (Zug, Vitt, & Caldwell, 2001), preventing their registration in herpetological studies. Similarly, range extensions of lizards were mainly from species that are rare or with arboreal habits, such as Diploglossus rozellae and Thecadactylus rapicauda (Campbell, 1998; Lee, 1996). In our study, however, range extensions for common species were also recorded (e.g., Anolis uniformis, Anolis pentaprion, Sceloporus teapensis, and Corytophanes cristatus), most probably because of the scarcity of surveys in the region and the small sampling effort. We also documented the range extension of Hemidactylus frenatus, an exotic species that is usually associated with human settlements, and hence, it can be easily overlooked in surveys carried out in forested habitats (Lee, 1996).

Overall, consistent with recent studies of small rodents (San-José, Arroyo-Rodríguez, & Sánchez-Cordero, 2014), mid- and large-sized mammals (Garmendia, Arroyo-Rodríguez, Estrada, Naranjo, & Stoner, 2013), primates (Arroyo-Rodríguez, González-Perez, Garmendia, Solà, & Estrada, 2013), and plants (Hernández-Ruedas et al., 2014), our study highlights that this region should be considered a priority area for biodiversity conservation. This region maintains the largest rainforest remnant in Mexico, and one of the most important in Mesoamerica (Dirzo & Robles-Gil, 1994). Unfortunately, it is increasingly deforested and fragmented. The annual deforestation rate in the region is between 1 and 8% (Couturier, Núñez, & Kolb, 2012; Mora, 2008), mainly to create agricultural and pasture lands. Management and conservation efforts should focus on preventing additional forest loss in the region, as: (1) many amphibians and reptiles are endemic to the Mayan forest; (2) the region shares <60% of the species with neighboring Mexican tropical forests, and (3) some species are particularly vulnerable to habitat loss and degradation (reviewed by Hernández-Ordóñez et al., 2014).

Acknowledgments

This research was supported by several grants from the Consejo Nacional de Ciencia y Tecnología (MABOTRO projects Semarnat-Conacyt 2002 C01-0597 and Sep-Conacyt CB-2005-01-510), and the Dirección General de Asuntos del Personal Académico (PAPIIT-DGAPA, UNAM; grants IN-227210, IA-203111, IB-200812 and RR-280812). We thank Gilberto, Fermín, Pascual, Miguel, Emanuel, Santos Jamangape, Martín Cervantes, and Ricardo Bolaños for their invaluable assistance in the field. We also thank Joseph Mendelson III (Department of Herpetology, Zoo Atlanta), Luis Canseco and Edmundo Pérez (Museo de Zoología de la Facultad de Ciencias, UNAM), and Alberto Cruz Silva (Colección Nacional de Anfibios y Reptiles, Instituto de Biología) for their help with the identification of collected specimens. Ricardo Bolaños assisted in the elaboration of the map. We also thank Luis Antonio Muñoz Alonso from the Colección Herpetológica de El Colegio de la Frontera Sur, Unidad San Cristóbal (ECOSUR-SC) for providing us invaluable information. OHO thanks Conacyt for his MSc and PhD scholarships. Idea Wild provided field equipment.