Amphibians and reptiles of the state of Durango, Mexico, with comparisons with adjoining states

Abstract A summary of the species of amphibians and reptiles of Durango, as well as their geographic distributions, habitat, and conservation status have been compiled. The herpetofauna of Durango consists of 36 species of amphibians and 120 species of reptiles. Durango shares the most species with Chihuahua (74.0%), and shares fewer species with Sinaloa (48.0%), Nayarit (48.7%), and Coahuila (48.0%). Arid-semiarid and Sierras habitat types have the most species, with valleys and Quebradas habitat types having fewer species. In Durango, there are several taxa of particular conservation concern including eleutherodactylid frogs, eublepharid, iguanid, phrynosomatid, and xantusid lizards, boid, colubrid, and natricid snakes, and emydid and testudinid turtles.


Introduction
Durango is located in central-northwestern Mexico, and covers 123,317 km 2 between 22°20'42"N, 26°50'42"N,and 102°28'22"W and 107°12'36"W (Fig. 1). It is the 4 th largest state in Mexico, representing 6.3% of the country's territory. Durango is bordered by Chihuahua to the north, Coahuila to the northeast, Zacatecas to the southeast, Nayarit to the southwest, and Sinaloa to the west (Figs 2-4). Durango has great biodiversity, a consequence of the combination of its geographical location and complex topography. The Tropic of Cancer passes through the southern part of the state, and the Sierra Madre Occidental runs from north to south dividing Durango into three large climatic regions (warm, temperate, and arid-semiarid). Winds from the Pacific Ocean interact with the Sierra Madre Occidental, producing a rain shadow that results in a significant humidity gradient in the state. This gradient results in a great contrast in the composition of species that inhabit the deep canyons of the western lowlands, the great elevations of the Sierra, the valleys of the foothills of the Sierra, and the arid-semiarid region of the eastern part of the state. The diversity of environmental conditions gives Durango a privileged place in terms of biodiversity. The state is home to dense forests of different timber species, such that, at the national level, Durango is the main producer of wood, contributing 28.5% of the total lumber production of the country (INEGI 2016). The Sierra Madre Occidental is considered a center of biodiversity in the North American continent, mainly due to its floral richness (Felger and Wilson 1994).
Topographically, Durango can be divided into four zones arranged (Fig. 1). In the westernmost zone adjacent to Sinaloa and Nayarit, ravines and canyons have formed through millions of years erosion by the rivers that run from the Sierra Madre Occidental to the Pacific Ocean. The southern part of this region is known as the Quebradas. To the east of the Quebradas is the Sierra region containing the mountainous massif of    Here, the list of amphibians and reptiles that have been recorded in the state of Durango to date is reported upon. While checklists of the herpetofauna of Durango are available (e.g., Valdez-Lares et al. 2013, 2017a, these earlier efforts are expanded upon by collecting and by summarizing the conservation statuses and their distributions within the state as well as the global distribution for each documented species. The herpetofauna of Durango is compared to those of the four adjoining states for which recent checklists are available (Chihuahua, Sinaloa, Nayarit, and Coahuila). Our goal is to place this checklist into a regional and conservation context not available in previous publications.

Materials and methods
A list of amphibians and reptiles of the state of Durango was compiled from the following sources: (1) our own field work; (2) specimens from the Herpetological Collection of CIIDIR-IPN-Durango; (3)   Species were included in the checklist only if the record was confirmed, either by direct observation or through documented museum records or vouchers in the state. Scientific names used in this publication are based on the taxonomic list published in Lemos-Espinal (2015). The amphibian names follow Frost (2017) or AmphibiaWeb (2017, see paragraphs below) and the reptile names follow Uetz and Hošek (2016). In addition, the conservation status of each species was recorded based on three sources: 1) the IUCN Red List 2017; 2) Environmental Viability Scores from Wilson et al. (2013a,b); 3) listing in SEMARNAT (2010). The following state lists were used to compare the species composition between Durango and the adjoining states: Chihuahua, Lemos-Espinal et al. (2017); Sinaloa, Enderson et al. (2009) Edwards et al. 2016). The number of overlapping species between each of these states and Durango was determined, and a cluster analysis used to examine the similarities among the herpetofaunas of Durango and its neighboring states (e.g., Enderson et al. 2009;Smith and Lemos-Espinal 2015). Acevedo et al. (2016) used two mitochondrial genes and 23 morphometric landmarks to evaluate the taxonomic status of Rhinella marina. They demonstrated that there were two separate evolutionary lineages within R. marina represented by two distinct morphotypes, one eastern and one western Andean. The concordance between the observed geographic patterns in morphometric and genetic traits support the recognition of two distinct species. The eastern populations retained the name R. marina, and the name R. horribilis was revalidated for the western populations. Duellman et al. (2016) treated two major clades as genera (Hyla, restricted to the Old World, and Dryophytes distributed primarily in the New World but with three species in Asia). Dryophytes is therefore used here. In addition, Sarcohyla bistincta was originally placed in the genus Hyla by Cope (1877), but was moved to the genus Plectrohyla by Faivovich et al. (2005). Duellman et al. (2016) performed a phylogenetic analysis of sequences from 503 species of hylid frogs and four outgroup taxa that resulted in a new phylogenetic tree of treefrogs. Among other results, a conservative new classification based on this tree has five new generic names, including Sarcohyla. This new genus contains 24 species, most of them from the Hyla bistincta and Hyla arborescandens groups of Duellman (2001), and includes the new combination Sarcohyla bistincta.

Recent taxonomic changes
The six species of ranid frogs that occur in Durango were long considered to be in the genus Rana, however, Frost et al. (2006) recommended the use of the name Lithobates, which was controversial. More recently, Yuan et al. (2016) retained all the species of these genera in the traditional genus Rana, based on a phylogenetic analysis of six nuclear and three mitochondrial loci sampled from most species of Rana, the lack of any diagnostic morphological characters for the genera recognized by Frost et al. (2006), and the clear monophyly of a larger group that include these genera. Rana is used here following Yuan et al. (2016) and AmphibiaWeb (2017). Montanucci (2015) studied the comparative morphology and color pattern variation of short-horned lizards (Phrynosoma douglasii species complex) using multivariate analyses of 20 morphological and color-pattern characters, and univariate statistics were summarized for 52 samples. The results of the morphological data analyses supported the recognition of P. douglasii as a distinct species, and the resurrection of P. brevirostris and P. ornatissimum as species distinct from P. hernandesi. He recognized two subspecies of P. ornatissimum: P. o. ornatissimum from central and southern New Mexico and western Texas; and P. o. brachycercum from the lower eastern slopes of the Sierra Madre Occidental and the adjacent plains in the Mexican states of Chihuahua, Durango, and Zacatecas. Tucker et al. (2016), based on Steyskal (1971), explained and justified why the genus name Aspidoscelis should be treated as masculine. Names used for species of Aspidoscelis occurring in Durango are thus A. costatus, A. gularis, A. inornatus, and A. marmoratus. Card et al. (2016) analyzed the genetic structure and phylogenetic relationships of Boa populations using mitochondrial sequences and genome wide SNP data obtained from RADseq, finding evidence that supports three widely-distributed clades roughly corresponding with western North America (Pacific Coast of Mexico), eastern North America (Atlantic Coast of Mexico and Central America), and South America. One of those clades represented the populations of the Pacific slopes of Mexico, from northern Sonora to west of the Isthmus of Tehuantepec. They resurrected the name sigma from the population described by Smith (1943) as Constrictor (= Boa) constrictor sigma from the María Madre Island, Tres Marías Islands, Nayarit, Mexico, which was regarded as a junior synonym of B. c. imperator by Zweifel (1960). Card et al. (2016) recognized the Boa populations from the slopes of the Mexican Pacific as Boa sigma, and this is followed here.

General distribution
Twenty-one of the 36 species of Amphibians that inhabit Durango are endemic to Mexico, 13 of them are limited to the Sierra Madre Occidental or to the Pacific Coast and the lowlands of the Sierra Madre Occidental (Table 1). Three more are species typical of the Mexican Plateau (Table 1). Another five have wide distributions that include parts of both Sierras Madre (Occidental and Oriental) and part of the Mexican Plateau (Table 1). Of the 15 amphibian species of Durango that are not endemic to Mexico, one is an introduced species (Rana catesbeiana), and eleven more are found in the USA and Mexico (Table 1). The remaining three species have a wide distribution from southern USA to Central or South America (Table 1).
Twenty-four of the 54 species of lizards that occur in the state are endemic to Mexico, one of them to the state of Durango (Xantusia bolsonae), three more have narrow distributions in northeastern Durango: Sceloporus maculosus limited to the Río Nazas drainage in Durango and Coahuila; Uma paraphygas limited to the Bolsón de Mapimí of southeastern Chihuahua, southwestern Coahuila, and northeastern Durango; and Xantusia extorris limited to northeastern Durango and adjacent Coahuila. Two more are restricted to small areas in the Sierra Madre Occidental: Sceloporus lemosespinali to eastern Sonora, northern Chihuahua, and extreme northwestern Durango; and S. shannonorum in central Durango to extreme northern Jalisco. Another ten species that occur in Durango and are endemic to Mexico are typical to the Pacific Coast and/or the Sierra Madre Occidental: Anolis nebulosus, Coleonyx fasciatus, Ctenosaura pectinata, Sceloporus Table 2. Summary of native species present in Durango by Family, Order or Suborder, and Class. Status summary indicates the number of species found in each IUCN conservation status in the order DD, LC, V, NT, E, CE (see Table 1 for abbreviations; in some cases species have not been assigned a status by the IUCN and therefore these may not add up to the total number of species in a taxon). Mean EVS is the mean Environmental Vulnerability Score, scores ≥ 14 are considered high vulnerability (Wilson et al. 2013a,b) and conservation status in Mexico according to SEMARNAT (2010) in the order NL, Pr, A, P (see Table 1 for abbreviations).  The remaining 30 species of lizards that inhabit Durango are not endemic to Mexico. Twenty-six of the non-endemics are species found in the USA and Mexico (Table 1). Three are found from northern Mexico to Central America (Table 1). The last one, Hemidactylus turcicus, is introduced to Durango.
Twenty-four of the 61 species of snakes that occur in Durango are endemic to Mexico. Two of them to Durango: Adelophis foxi and Thamnophis nigronuchalis. Thirty snake species that are found in Durango are distributed from the USA to Mexico (Table 1). Five more species are found from central or southern USA to Central or South America (Table 1). One species ranges from Mexico to northeastern South America: Masticophis mentovarius. The last species that inhabits Durango and is not endemic to Mexico is an introduced species to Mexico, Indotyphlops braminus.
Three of the five species of turtles that inhabit Durango are endemic to Mexico, two to the Bolsón de Mapimí in southeastern Chihuahua, southwestern Coahuila, and northeastern Durango: Kinosternon durangoense and Gopherus flavomarginatus. The other is widely distributed in the lowlands of western Mexico and throughout the central and southern portion of the Mexican Plateau: Kinosternon integrum (it is not native to the Valley of Mexico but has been introduced there). The two non-endemic species of turtles are found from southwestern USA to northern Mexico: Trachemys gaigeae and Kinosternon hirtipes. Table 3. Summary of the number of native species (% of total number of species of taxonomic group in Durango in parentheses) in different taxonomic groups found in different habitat types in Durango, Mexico (see text for description of the habitat types).

Habitat types
The Sierra habitat type (46.1%) and the arid-semiarid habitat type (42.8%) had the highest percentages of the herpetofauna in Durango, whereas both the valley (29.9%) and Quebradas (24.0%) habitat types had a lower percentage (Table 3). For amphibians alone, the Sierra habitat type had slightly more than 50% of the species in Durango (52.8%) followed by the valley habitat type (41.7%) and Quebradas habitat type (30.6%). As might be expected, the arid-semi-arid habitat type had the fewest amphibian species (19.4%; Table 3). This distribution of species is also found when examining anuran species (Table 3). For salamanders, species are almost exclusively found in the Sierra habitat type, with one species found in the valley habitat type, and none in the arid-semi-arid and Quebradas habitat types (Table 3). Reptiles showed a different pattern, with the most species being found in the arid-semiarid habitat type (50%) and the Sierra habitat type (44.1%), with the valleys (26.3%) and the Quebradas (22.0%) having fewer species. This pattern is found in both lizards and snakes (Table 3), and is primarily driven by the most diverse families in these groups (e.g., Phrynosomatidae, Colubridae, and Natricidae). Turtles are found in the four habitat types with 80% of the species occurring in the arid-semiarid habitat type and less than half of the species found in the other three habitat types.

Comparisons with neighboring states
Overall, Durango shares the most species with Chihuahua (Table 4). This holds true for amphibians; however, Durango shares almost as many species of amphibians with Sinaloa and Nayarit as with Chihuahua. For reptiles, Durango and Chihuahua share the most species by a large margin over the other states (Table 4). The cluster analysis recovered the same tree structure for Durango and its neighboring states when the entire herpetofauna, reptiles, and amphibians are each considered ( Figure 5). In each . Such results suggest that the conservation of the herpetofauna of this region will need habitat specific conservation plans that cross state borders and will require integration of state, regional, and country-level efforts.

Conservation status
Overall, 7.6% of the amphibian and reptile species were IUCN listed (i.e., Vulnerable, Near Threatened, Endangered, or Critically Endangered), but 33.3% were placed in a protected category by SEMARNAT and 29.3% categorized at high risk by the EVS (Tables 1, 2). For amphibians, 12.1% were IUCN listed, 31.4% protected by SEMARNAT, and 20% at high risk according to the EVS (Tables 1, 2). For reptiles, 6.1% were listed in IUCN, 33.9% protected by SEMARNAT, and 32.2% at high risk by EVS. These results suggest that the herpetofauna of Durango is considered to be of relatively low conservation concern at a global scale, but at a national level, there is much greater conservation concern. There are several taxa that, based on their IUCN listing, SEMARNAT category, or their EVS, are of conservation concern. Families that include species of particular conservation concern include Eleutherodactylidae, Eublepharidae, Iguanidae, Phrynosomatidae, Xantusidae, Boidae, Colubridae, Natricidae, Emydidae, and Testudinidae (Tables 1, 2). The IUCN, SEMARNAT, and EVS categories are based on global or country-level assessments, and it is likely that there are amphibians and reptiles whose conservation status in Durango is not accurately assessed by the global level assessment. Additional assessments at the state level in Durango, and other Mexican states, are needed to establish conservation or management needs for states, or even regions.
To help determine which habitat types within Durango may house species of particular conservation concern, the conservation statuses of reptile and amphibian taxa in each habitat type found in Durango was summarized. None of the amphibians in the arid-semiarid habitats and Quebradas were in protected IUCN categories (VU, NT, EN, CE), 7.1% in the valleys, and 25% in the Sierra habitat. For SEMARNAT categories, 42.8% of amphibians in the arid-semiarid habitats, 26.7% in the valleys, 33.3% in the Sierra habitat, and 18.2% in the Quebradas were listed. For EVS, 100% of the amphibians in the arid-semiarid habitat were in the low category. Almost half (46.6%) of the amphibians in the valley habitat were in the low category, 40% in the medium category, and 13.3% in the high category. In the Sierra habitat type, 26.3% of amphibians were in the low category, 42.1% in the medium, and 31.6% in the high. For the Quebradas habitat, 45.4% were in the low and medium categories and 9.1% in the high. Based on this summary, it is clear that for amphibians, the Sierra habitat has the most at risk species and the arid-semiarid habitat has relatively fewer at risk species. For amphibians, therefore, the Sierra habitat would appear to be a priority target for conservation efforts.
For the IUCN listings, all habitat types had relatively few species of reptiles in the protected categories (arid-semiarid, 8.5%; valleys, 3.2%; Sierra, 3.8%; and Quebradas, 7.7%). However, 39% of reptiles in the arid-semiarid habitat, 41.9% from the valley habitat, 42.3% from the Sierra habitat, and 30.8% from the Quebradas habitat were in the protected SEMARNAT categories. For the arid-semiarid habitat type, 28.1% of reptiles were in the low EVS category, 43.8% in the medium, and 28.1% in the high. In valleys, 29% of the reptiles were in the low, 51.6% in the medium, and 19.4% in the high. Of the reptiles in the Sierra habitat type, 21.6% were in the low, 45.1% in the medium, and 33.3% in the high categories. For the Quebradas habitat type, 19.2% were in the low EVS category, 50% in the medium, and 30.8% in the high. In contrast to amphibians, at risk reptile species are more evenly distributed across the habitat types. Therefore, conservation efforts for reptiles should address all habitat types.
Three non-native species of amphibians and reptiles were documented in Durango: R. catesbeiana, H. turcicus, and I. braminus. Non-native species can negatively affect native herpetofaunal communities in Mexico (see Wilson and Townsend 2010). Of the three non-native species, R. catesbeiana is of particular concern. Rana catesbeiana is known to have many impacts on native communities as a competitor, predator, and disease vector on a global scale (reviewed in Moutou and Pastoret 2010;Kraus 2015), as well as in Mexico (e.g., Luja and Rodriguez-Estrella 2010;Becerra Lopez et al. 2017). The potential impacts of H. turcicus are less well documented, but its congener H. frenatus has affected native herpetofauna through competition (reviewed in Punzo 2005;Kraus 2015). The impacts of I. braminus are, to our knowledge, unstudied, even though it has been widely introduced around the world (see Borroto-Páez et al. 2015).
There is thus the potential for these non-native amphibians and reptiles to have negative impacts on the native herpetofauna, and other organisms, of Durango. The extent of these potential impacts need to be evaluated further.
Hopefully, this list of amphibian and reptile species in Durango with their global and country-level conservation statuses will prompt further investigations into the herpetofauna of this state, which could provide the needed information to allow for stateor regional-specific, or even habitat type, conservation measures to be undertaken.