Amphibians and reptiles of the state of Hidalgo, Mexico

We compiled a checklist of the amphibians and reptiles of the state of Hidalgo, Mexico. The herpetofauna of Hidalgo consists of a total of 175 species: 54 amphibians (14 salamanders and 40 anurans); and 121 reptiles (one crocodile, five turtles, 36 lizards, 79 snakes). These taxa represent 32 families (12 amphibian families, 20 reptile families) and 87 genera (24 amphibian genera, 63 reptile genera). Two of these species are non-native species ( Hemidactylus frenatus Dumeril and Bibron, 1836 and  Indotyphlops braminus  (Daudin, 1803)). This herpetofauna represents a mixture of species from both the Sierra Madre Oriental and the Transvolcanic Belt. In addition, 26% of all categorized amphibian and reptile species in Hidalgo are considered Vulnerable, Near Threatened, Endangered, or Critically Endangered by the IUCN Red List. Thus, Hidalgo represents a relatively unique and threatened diversity of amphibians and reptiles.


INTRODUCTION
Hidalgo is one of the smallest states in Mexico; ranking 26 th out of 31 states, with a surface area of 20,905 km 2 , which represents 1.1% of the surface area of the country. The topography of Hidalgo is very rugged, its lowest point is a few meters above sea level and its highest point is over 3,300 m above sea level. Parts of three physiographic provinces are found in the state: the Sierra Madre Oriental; the Transvolcanic Belt; and the North Gulf Coastal Plain.
Much of Hidalgo is subject to severe human pressures such as extraction of timber, agriculture, animal husbandry, and expansion of human settlements, so that more than 60% of the native vegetation has been transformed into some kind of anthropogenic habitat. Almost the entire southern half of the state (i.e., the area occupied by the Transvolcanic Belt province) has been modified by the establishment of agricultural crops. At higher elevations in the provinces of Sierra Madre Oriental and the Transvolcanic Belt, there are conifer forests of pine (Pinus spp.), oak (Quercus spp.), and Mexican Fir (Abies religiosa (Kunth) Schlechtendahl and Chamisso, 1830), among other species. In the lower areas of these provinces is mountain cloud forest characterized by the most diverse vegetation type per unit area of the country (Rzedowski 1996). The cloud forest of the mountains on the outskirts of the village of La Mojonera is home to the most important Fagus grandifolia spp. mexicana (Martínez) forest in the country. Fagus grandifolia spp. mexicana (Martínez) is a relict taxon whose distribution in Mexico represents relictual areas worthy of greater attention in biogeographic and conservation studies (Alcántara-Ayala and Luna-Vega 2001). Such cloud forests in Mexico are also under threat from climate change (Ponce-Reyes et al. 2012).
The complex topography of Hidalgo, along with the climates and vegetation types present, has resulted in great faunal diversity that has caught the attention of biologists. In recent years there have been important contributions that have attempted to summarize and describe some groups of reptiles or the entire herpetofauna of Hidalgo (e.g., Bryson and Mendoza-Quijano 2007;Valencia-Hernández et al. 2007;Ramírez-Bautista et al. 2010, of specific areas, habitats or localities within Hidalgo (e.g., Fernandez-Badillo and Goyenechea Mayer-Goyenechea, 2010;Vite-Silva et al., 2010;Huitzel-Mendoza and Goyenechea Mayer-Goyenechea 2011;Cruz-Elizalde and Ramírez-Bautista 2012;Hernández-Salinas and Ramírez-Bautista 2013). Indeed, there appears to be a new interest in the herpetofauna of Hidalgo, as epitomized by several recent range extensions or rediscoveries of snakes (Roth-Monzon et al. 2011;Berriozabal-Islas et al. 2012;Ramírez-Bautista et al. 2013;Badillo-Saldaña et al. 2014;Lara-Tufino et al. 2014), salamanders (Badillo-Saldaña et al. 2015) and crocodilians (Mejenes-López and Hernández-Bautista 2013), and the description of a new species of lizard in the genus Xenosaurus (Woolrich-Piña Lemos-Espinal and Smith | Herpetofauna of Hidalgo, Mexico bordered by Querétaro, San Luis Potosí, and Veracruz; to the south by Puebla, Tlaxcala, and México; to the east by Veracruz and Puebla; and, to the west, by México and Querétaro. The province of the Sierra Madre Oriental in Hidalgo is represented by the subprovince of Carso Huasteco, so named for possessing features of a major karst topography (INEGI 2009). This province is divided by important rivers, such as Acoyoapa, Amajac, Atlapexco, and Candelaria, flowing through it. The highest elevations in this region exceed 2,000 m above sea level. This region is dominated by limestone. Within the state of Hidalgo, this province covers approximately 9,713 km 2 (46.46% of the state surface area) and occupies approximately the northern half of the state. In this portion of the Carso Huasteco, mountain ranges dominate. Its lowest areas are localized in the north and northeastern part of the and Smith 2012). Cruz-Elizalde et al. (2015) have also recently evaluated the effectiveness of protected areas in conserving the herpetofauna of Hidalgo.
The goal of this publication is to report on the list of the amphibians and reptiles known to occur in the state of Hidalgo. We hope that this publication will help to increase the knowledge of these two classes of tetrapods and encourage the development of future work on them in this small, but biologically important Mexican state, especially given the extensive conversion of Hidalgo's landscape to agricultural purposes.

Study site
Hidalgo is located in the central part of Mexico, between latitudes 21°24ʹ and 19°36ʹ N and longitudes 097°58ʹ and 099°53ʹ W (Figure 1). To the north it is Lemos-Espinal and Smith | Herpetofauna of Hidalgo, Mexico state and constitute the region known as Huasteca Hidalguense, where the topographical systems classified as "lying valley slopes" are common (INEGI 2009).
In Hidalgo, the Transvolcanic Belt province occupies a surface area of approximately 11,136 km 2 and represents 53.27% of the state's surface area. It occupies slightly more than the southern half of the state and contains two subprovinces: 1) Coastal and Mountain Regions of Querétaro and Hidalgo. This subprovince runs from west to east as low hills of volcanic material, < 2,000 m elevation, which is essentially enclosed on all sides by a system of mountains, plateaus, and hills, almost all of which have a volcanic origin. Only one peak, the Nopala, has an altitude > 3,000 m; and 2) Lakes and Volcanoes of Anáhuac that enters the southern part of Hidalgo and occupies 15.86% of the state's surface area (INEGI 2009).
The province of the North Gulf Coastal Plains covers approximately 56 km 2 of the surface area of Hidalgo (= 0.27%). It occupies a small portion of the northeastern corner of the state in parts of the municipalities of Huautla and Huehuetla (INEGI 2009).

Data collection
We obtained the list of amphibians and reptiles of the state of Hidalgo from the following sources: (1) specimens from the Laboratorio de Ecología-UBIPRO (LEUBIPRO) collections; (2) databases from the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (National Commission for the Understanding and Use of Biodiversity; CONABIO), that were the results of various scientific projects undertaken by this institution in Hidalgo and includes museum records from the principal museum collections in Mexico and the United States which include the following 22 collections: Departamento de Zoología, Escuela Nacional de Ciencias Biológicas, I.  Woodall (1941); and (4) our personal field work, primarily focused around the municipalities of Molango, San Agustín Metzquititlán, Tlanchinol, and Zacualtipán. We visited this region periodically from 2002 to 2014, taking notes on the amphibians and reptiles observed during visual encounter surveys. All relevant Mexican laws and regulations pertaining to observation and collection of reptiles and amphibians were followed during these surveys.
Species were included in the checklist only if we were able to confirm the record, either by direct observation or through documented museum records or vouchers in the state. Species with a questionable distribution in Hidalgo, or those that are mentioned in the literature without documented support of their presence in the state were not included in our list. In addition, we recorded the conservation status of each species based on three sources: 1) the IUCN Red List, 2) Environmental Viability Scores from Wilson et al. (2013a,b), and 3) listing in SEMARNAT (2010).
Fourteen more of the species endemic to Mexico that are found in Hidalgo have a peculiar distribution occupying the Sierra Madre Occidental as well as the Sierra Madre Oriental and parts of either the Mexican Plateau or the Transvolcanic Belt. They consist of one salamander (Pseudoeurycea bellii (Gray, 1850)), three anurans (Incilius marmoreus (Wiegmann, 1833), Eleutherodactylus nitidus (Peters, 1870) and Plectrohyla bistincta (Cope, 1877)), two lizards (Phrynosoma orbiculare (Linnaeus, 1758)  Thirty-three of the 83 non-endemic species reach their northernmost distribution in Mexico and their southernmost distribution in Central America or South America, including four anurans, one crocodile, two turtles, six lizards, and 20 snakes.
Another 19 species found in Hidalgo have a wide distribution that ranges from Canada or the United States to Central America or South America. These taxa represent five anurans, two lizards, and 12 snakes. Two species that inhabit Hidalgo are not native to the Western Hemisphere: one lizard introduced from southeastern Asia (Hemidactylus frenatus Duméril and Bibron, 1836), and one snake introduced from southern Asia (Indotyphlops braminus (Daudin, 1803)).
When comparing the species list of Hidalgo with those of neighboring states for which recent checklists are available, we found substantial overlap of species. Hidalgo and Puebla share 118 total species (40 amphibians and 78 reptiles), representing 48.2% of the total species, 49.4% of the amphibians, and 47.6% of the reptiles found in Puebla. There were 65 total species shared between Hidalgo and México, with 21 amphibian species and 44 reptile species shared. These represent 45.4%, 42%, and 47.3% of the total species, amphibian species, and reptile species of México, respectively. San Luis Potosí and Hidalgo share 132 total species, or 72.9% of the species found in San Luis Potosí. These two states share 36 species of amphibians and 96 species of reptiles, which represent 85.7% and 69.1% of the amphibian and reptile species found in San Luis Potosí, respectively. Querétaro shares 101 total species, 24 amphibian species and 77 reptile species with Hidalgo. These represent high percentages of the species found in Querétaro (86.3% total species, 82.8% amphibian species, 87.5% reptile species).

Lemos-Espinal and Smith | Herpetofauna of Hidalgo, Mexico
Twelve percent of all categorized herpetofaunal species in Hidalgo are either Critically Endangered or Endangered, and 26.2% are categorized as Vulnerable, Near Threatened, Endangered, or Critically Endangered by the IUCN. Using the EVS of Wilson et al. (2013a, b), 24.8% (43 of 173) were placed in the high vulnerability category (EVS > 14). According to the SEMARNAT (2010) list, 1.7% of Hidalgo's species are in danger of extinction (P), 18.4% are threatened (A), 27.6% are subject to special protection (Pr), and 52.3% are not listed. In addition, of those species for which population trends were described, 31% had declining populations according to the IUCN Red List.

DISCUSSION
The list of species of amphibians and reptiles we have generated for Hidalgo demonstrates the potential importance of this small state for the Mexican herpetofauna. More than half of the species of amphibians and reptiles found in Hidalgo are endemic to Mexico, including four that are endemic to Hidalgo. Several of these endemics have a relatively narrow distribution in Mexico; thus, Hidalgo represents an important component of their range. Our compilation of the conservation status and population trends of its herpetofauna also confirms that Hidalgo is of potential importance for several taxa. For example, 12 salamanders in the family Plethodontidae occur in Hidalgo, of which 3 are endemic to Hidalgo and the other 9 are endemic to Mexico. Four of the 12 species are listed as Critically Endangered and 3 are listed as Endangered by the IUCN (see Tables 1, 2). One of the 3 Hidalgo endemic species are listed as Critically Endangered, one as Endangered, and one as Data Deficient by the IUCN. All but one of the Plethodontidae has an EVS that places them in the high vulnerability category (Table 1; Wilson et al. 2013a). Three are listed as threatened (A) and one as in danger of extinction (P) in SEMARNAT (2010). In addition, ten of the plethodontid species have a negative population trend (the remaining 2 have unknown trends). Although the salamanders in the family Plethodontidae are in particular danger, as they are elsewhere in Mexico (see Frías-Alvarez et al. 2010;Wilson et al. 2013a), Hidalgo is home to several other Endangered and Critically Endangered species (see Tables 1, 2). The herpetofauna of Hidalgo therefore includes many species of conservation concern, with taxa of particular concern (based on IUCN listing and EVS) including Plethodontidae, Eleutherodactylidae, Crocodylia, Emydidae, Anguidae, Xenosauridae, Elapidae, and Viperidae (see Table 2). Our compilation also found many species for which no IUCN or SEMARNAT (2010) classification were given and many other species (43 of the 173 native species; 24.8%) had no information on population trends. However, all of these species have received EVS scores from Wilson et al. (2013a, b). It is therefore critical that the herpetofauna of Hidalgo be studied further to establish population status and trends.
Hidalgo also appears to represent a "mixing-pot" for species whose distributions are from the Sierra Madre Occidental and the Transvolcanic Belt, as is evidenced by the overlap in species found in neighboring states, especially Querétaro and San Luis Potosí. Unfortunately, much of Hidalgo has been or is being converted to human-dominated or human-altered habitats. We hope that this checklist, along with other recent works describing and studying the herpetofauna of Hidalgo (see Introduction), will help highlight the diversity of reptiles and amphibians that can be found in this small but biologically important Mexican state.