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

Abstract Chihuahua is Mexico’s largest state, and its physiographic complexity affects the distribution of its herpetofauna. We list amphibians and reptiles for the state of Chihuahua, with their conservation status. We also compare this list to those of six adjoining states in the United States and Mexico (New Mexico, Texas, Coahuila, Durango, Sinaloa, and Sonora). A total of 175 species of amphibians and reptiles is found in Chihuahua. Thirty-eight are amphibians, and 137 reptiles. Chihuahuan amphibians and reptiles represent just over 37% of such species from Chihuahua and neighboring states. Chihuahua shares the highest proportion of its herpetofauna with Sonora and Durango. Most of the herpetofauna of Chihuahua falls in IUCNs least concern category and is not listed by SEMARNAT. However, turtles in Chihuahua are a group of particular conservation concern.


Introduction
Chihuahua is the largest state in Mexico. Its 245,612 km 2 (lying between 25°38'N to the south, 31°47'N to the north, and between 103°18'W to the east, and 109°7'W to the west) represent 12.6% of the total territory of the nation. Chihuahua is physiographically complex (Fig. 1), and this complexity affects the distribution of the herpetofauna.
The western part of the state is primarily occupied by the Sierra Madre Occidental, which passes the Continental Divide, separating the Pacific and Atlantic drainages. In Chihuahua, the Sierra Madre varies in width from ~130-160 km in the south (west of Hidalgo de Parral) to ~65-80 km in the north (west of Casas Grandes) (Tanner 1985, Lemos-Espinal andH. Smith 2007). The topography of the Sierra Madre Occidental of Chihuahua is very heterogeneous. The highest altitude is on Cerro Mohinora, at 3,300 m, and the extreme southwestern Pacific slopes of this Sierra are characterized by deep canyons that drop down to ~250 m in the Barranca del Septentrión/Cañón de Chínipas, making diverse habitats for plants and animals. Copper Canyon is a 64,750 km 2 system of six interconnected canyons located in Southwestern Chihuahua. Four of these six canyons are deeper than the Grand Canyon, some by over 305 m. The deepest canyon is Urique Canyon, 1,870 m in depth; Batopilas Canyon is 1,830 m deep; Sinforosa Canyon is 1,800 m deep; and Copper Canyon is 1,759 m deep (Martin et al.1998, INEGI 2004, Wyndham 2004, Lemos-Espinal and H. Smith 2007, http://www.earlham.edu/~garcier/Geology/coppercanyon.htm).
Over half of the state of Chihuahua, east of the Sierra Madre, is covered by high plains at ~1,200-1,700 m. From these plains arise a large number of small to medium-sized, isolated sierras, some of which reach altitudes of over 2,000 m. Some are high enough to support coniferous forests, constituting continental "islands" surrounded by a "sea" of semiarid plains, where differentiation among populations is enhanced by isolation.
In extreme northeastern Chihuahua, deep canyons, similar to those on the Pacific side of the Sierra Madre Occidental, cut into the edge of the high plains, and support their own distinct herpetofaunal assemblages. Among them is the great Cañón de Santa Elena, in the Zona de Protección de Flora y Fauna Silvestre Cañón de Santa Elena, an extension of the Big Bend National Park of the United States.
Although there has been a considerable interest in the herpetofauna of Chihuahua, as stated above, none of these 163 publications has focused on the conservation statuses of the documented species for this state. Here, we report the list of amphibians and reptiles that have been recorded so far for the state of Chihuahua. While checklists for Chihuahua are available (e.g., Lemos-Espinal andH. Smith 2007, 2015a), we expand on these earlier efforts by also collecting and summarizing the conservation statuses for each documented species. We also com pare the list of the six adjoining states in the United States and Mexico for which recent checklists are available (New Mexico, Texas, Coahuila, Durango, Sinaloa, and Sonora). Our goal is to place this checklist into a regional and conservation context not available in previously published checklists.
Herpetology, Kansas University (MNHUK); and (4) a thorough examination of the available literature on amphibians and reptiles in the state. 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. 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).
Scientific names used in this publication are based on the taxonomic list published in Lemos-Espinal (2015). The amphibian names follows Frost (2016) and the reptile names follows Uetz and Hošek (2016). State lists used to compare the species composition between Chihuahua and the adjoining states were: Dixon (2015) for Texas; Enderson et al. (2009) [Baird & Girard]). We also determined the number of overlapping species between each of these states and Chihuahua.

General distribution
Thirteen of the 38 species of amphibians that inhabit Chihuahua are endemic to Mexico, one of them (Lithobates lemosespinali) is restricted to a small area in the Sierra Madre Occidental of Chihuahua, and another (Isthmura sierraoccidentalis) is found only in an isolated population in the Sierra Madre Occidental of Sonora and Chihuahua. Eleven Table 1. Checklist of amphibians and reptiles of Chihuahua providing the habitat type (CD = Chihuahuan Desert, SMO = Temperate Forests of the Sierra Madre Occidental, SBT = Subtropics -Canyons of the Sierra Madre Occidental; GEN = Generalist -occupies more than one habitat type), IUCN Status (DD = Data Deficient; LC = Least Concern, V = Vulnerable, NT = Neat Threatened; E = Endangered; CE = Critically Endangered) according to the IUCN Red List (The IUCN Red List of Threatened Species, Version 2016.1; www.iucnredlist.org; accessed 30 June 2016), Environmental Vulnerability Score (EVS; the higher the score the greater the vulnerability; NE = not evaluated) from Wilson et al. (2013a,b) and Johnson et al. (2015a), and conservation status in Mexico according to SEMARNAT (2010) (P = in danger of extinction, A = threatened; Pr = subject to special protection, NL -not listed). Source denotes whether the species was observed in the field by the authors (A), documented in the CONABIO data base and/or museum collections (C/M), or found in the literature (citation of source). Five of the 13 species of turtles that inhabit Chihuahua are endemic to Mexico, two of them to the Bolsón de Mapimí, a small area in southeastern Chihuahua, southwestern Coahuila, and northeastern Durango (Kinosternon durangoense and Gopherus flavomarginatus), two more to western Mexico (Terrapene nelsoni and Kinosternon integrum), and one more to the subtropics of southeastern Sonora, southwestern Chihuahua, and northern Sinaloa (Gopherus evgoodei). Six more species occur from central or southern United States to northern (Terrapene ornata [Fig. 3], Trachemys gaigeae, Kinosternon flavescens, and K. sonoriense) or central or southern Mexico (Kinosternon hirtipes  Table 2. Summary of species present in Chihuahua by family, order or suborder, and class. Status sum mary 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).

Class
Order   and Apalone spinifera). The remaining two species of turtles are widely distributed from southern Canada to northern Mexico (Chrysemys picta) and from southeastern Sonora, through the Pacific Coast, to Costa Rica (Rhinoclemmys pulcherrima). Fifteen of the 51 species of lizards that occur in Chihuahua are endemic to Mexico, two of them to the state of Chihuahua (Barisia levicollis [ Fig. 4] and Plestiodon multilineatus), one of the remaining 13 endemics is limited to the Bolsón de Mapimí (Uma paraphygas), one more to a small area in eastern Sonora and western Chihuahua (Sceloporus lemosespinali), another one to the temperate forests of western Chihuahua and northern Durango (Plestiodon bilineatus), one more to the Chihuahua Desert from northern Chihuahua to central Mexico (Holbrookia approximans), two others occupy areas in the Sierra Madre Occidental and the Sierra Madre Oriental (Barisia ciliaris), and even the Transvolcanic Belt (Phrynosoma orbiculare).  Agkistrodon contortrix,Crotalus atrox,C. lepidus,C. molossus,C. ornatus,C. pricei,C. scutulatus,C. viridis,and C. willardi [Fig. 5]). Another four species range from northern Mexico to Central or even South America  In terms of habitat types, 47 species are found in the temperate forests of the Sierra Madre Occidental. Forty-four are found in the subtropical canyons of the Sierra Madre Occidental. Fifty-eight species are found in the Chihuahuan Desert. One species is found in SON. Twenty-five species occupy more than one habitat type (i.e., are generalists).

Likely species and poorly documented species
There are several additional species that are likely to occur in Chihuahua, but that have not been recorded within the state. Three species of anurans might occur in the deep canyons and lowlands of the extreme southwestern part of the state. The Pacific Stream Frog (Craugastor vocalis) was recorded by Hardy and McDiarmid (1969) in extreme northeastern Sinaloa, 16 km NNE Choix, 520 m, near the state line with Chihuahua. The Sabinal Frog (Leptodactylus melanonotus) was recorded by Bogert and Oliver (1945) from Güirocoba and Álamos, Sonora, only about 25 and 35km respectively from the Chihuahua border, and by Smith et al. (2005) from the Río Mayo at the gates of Presa Mocuzari, Sonora. Hardy and McDiarmid (1969) mapped localities for this species (as L. occidentalis, a junior synonym) from throughout the lowlands of Sinaloa, including a locality in the extreme northeastern corner. The Lowland Burrowing Treefrog (Smilisca fodiens) has been recorded close to Chihuahua by Hardy and McDiarmid (1969) for Sinaloa, Bogert and Oliver (1945) for Sonora, and Trueb (1969) and Duellman (2001) for both states. Another anuran species likely to occur in extreme northeastern Chihuahua is the Gulf Coast Toad (Incilius nebulifer). This species of toad is represented by isolated populations at the southern extremity of the Big Bend region of Texas, adjacent to Coahuila (Conant and Collins 1998).
It is likely that at least four other turtle species occur in Chihuahua. Three species have been taken close to the state line with Sonora and Sinaloa, in the extreme southwestern part of the state. Kinosternon alamosae has been taken in the vicinity of Álamos, Sonora, about 35 km from the Chihuahua border. Trachemys hiltoni has been recorded from Güirocoba, ~25 km from Chihuahua, and from extreme northern Sinaloa (Hardy and McDiarmid 1969). Seidel (2002) mapped its range into Chihuahua, but only conjecturally. Legler and Webb (1970) stated that the species is limited to the Río El Fuerte drainage. These last authors stated that Trachemys yaquia is limited to the drainages of the Río Mayo, Río Sonora and Río Yaqui, however, Seidel (2002) conjectured that the range of this species extended into Chihuahua. In addition, the Common Snapping Turtle (Chelydra serpentina) occurs in the Río Grande at least in New Mexico (Degenhardt et al. 1996), and may well occur farther south in extreme northeastern Chihuahua, where little turtle trapping has been done.
There are at least nine lizard species not yet recorded in the state of Chihuahua that are likely to occur in it; four of them in the deep canyons and lowlands of extreme southwestern Chihuahua; three in the extreme northeastern part of the state; and two in the extreme northwestern part. The Zebra-tailed Lizard (Callisaurus draconoides) was recorded by Bogert and Oliver (1945) from Güirocoba and Álamos, Sonora (~25 and 35 km respectively from the Chihuahua border), and Hardy and McDiarmid (1969) spotted it at several localities in extreme northeastern Sinaloa. The Black Banded Gecko (Coleonyx fasciatus) has been recorded from five localities along the foothills of the Sierra Madre Occidental of eastern Sonora, three of these localities are in the Álamos region, one fairly close to Chihuahua. Its habitat suggests that it might occur in some of the deep canyons of southwestern Chihuahua. The Regal Horned Lizard (Phrynosoma solare) ranges from southern Arizona through almost all of Sonora, into northern Sinaloa. Hardy and McDiamid (1969) and Bogert and Oliver (1945) recorded it near Chihuahua in both Sinaloa and Sonora. It is a species of arid and semiarid habitats on plains, hills, and low mountain slopes. The Desert Spiny Lizard (Sceloporus magister) shows a range similar to that of the preceding species. East of the Sea of Cortés, it is the western representative of the eastern S. bimaculosus.
In northeastern Chihuahua the presence of three additional lizard species is likely. Wright (1971) indicated that the New Mexico Whiptail (Aspidoscelis neomexicana) is known from only central New Mexico and extreme southwestern Texas; almost all records are from near the Río Grande. He projected its range into Chihuahua along the Río Grande; although there are no records, its occurrence is highly likely there. Conant and Collins (1998) depicted the southern part of the Big Bend region of Texas as part of the range of the Reticulate Banded Gecko (Coleonyx reticulatus). It may be expected in adjacent parts of Chihuahua. Also Conant and Collins (1998) projected the range of the Texas Alligator Lizard (Gerrhonotus infernalis) to include the southern part of the Big Bend region of Texas, southward through eastern Chihuahua, most of Coahuila and other states to the south. In northwestern Chihuahua the presence of the Western Banded Gecko (Coleonyx variegatus) is expected. As indicated in Stebbins (2003) and Degenhardt et al. (1996), this species occurs in extreme southwestern New Mexico, and probably also in adjacent northwestern Chihuahua. The Gila Monster (Heloderma suspectum) is also expected to occur in this part of the state. The known occurrence of this species in Sonora, Arizona, and New Mexico close to the Chihuahua border indicates that occurrence in Chihuahua is likely.
It is highly likely that nine more snake species occur within the state of Chihuahua. Two of them in southwestern Chihuahua (Phyllorhynchus browni and Pseudoficimia frontalis); four in northeastern Chihuahua (Coluber constrictor, Lampropeltis alterna, Pantherophis bairdi, Tantilla cucullata); two in the northwestern part of the state (Crotalus tigris, Sistrurus catenatus); and one in extreme southeastern Chihuahua (Tantilla atriceps). The Saddled Leaf-nosed Snake (Phyllorhynchus browni) was recorded by Bogert and Oliver (1945) from Alamos, ~35 km from the Chihuahua border; Hardy (1972) reviewed the distribution of The False Ficimia (Pseudoficimia frontalis), citing specimens from near Álamos and Güirocoba, Sonora, ~35 and 25 km from the Chihuahua border, respectively. The North American Racer (Coluber constrictor) is rare in Mexico, with only three records. Two are from Coahuila, including one from the extreme northwestern corner, in the Sierra del Carmen (Wilson 1966). Occurrence in Chihuahua seems likely. The Gray-banded Kingsnake (Lampropeltis alterna) is well known in the Big Bend of Texas, and elsewhere in that state, as well as in Coahuila and other adjacent states in Mexico, but it has never been found in Chihuahua, although it almost certainly occurs there. Baird´s Ratsnake (Pantherophis bairdi) occurs in western Texas, including the Big Bend region, as well as northern Coahuila (Conant and Collins 1998); it is highly likely to occur in adjacent Chihuahua. The Trans-Pecos Blackheaded Snake (Tantilla cucullata) is known only in Texas, in the Big Bend and immediate vicinity (Dixon et al. 2000); occurrence in adjacent Coahuila and Chihuahua is to be expected. In northwestern Chihuahua the occurrence of the Tiger Rattlesnake (Crotalus tigris) is expected. Stebbins (2003) indicates occurrence of this species in the extreme southeastern corner of Arizona, and in eastern Sonora near the Chihuahua border. An inhabitant of arid and semiarid foothills deserts, it may enter the latter state in some of its semiarid valleys. Another rattlesnake, the Massasagua (Sistrurus catenatus), is known from southern New Mexico (Degenhardt et al. 1996) and southeastern Arizona (Brennan and Holycross 2006); it likely occurs in adjacent Chihuahua. In extreme southeastern Chihuahua the occurrence of the Mexican Black-headed Snake (Tantilla atriceps) is expected. The known range of this species comes close to the southeastern corner of the state (Cole andHardy 1981, Conant andCollins 1998).

Comparisons with neighboring states
Overall, the species of amphibians and reptiles in Chihuahua represent just over 37% of the total pool of species from Chihuahua and its neighboring states (Tables 3, 4). Species of reptiles from Chihuahua make up even more of the total pool of species, especially the Squamata, and more specifically Anguids and Snakes. Chihuahuan amphibians make up less of the species pool, especially salamanders. Chihuahua has a good proportion of the region's Ambystomatid salamanders, but is very depauperate in Plethodontids.
Overall, Chihuahua shares the highest proportion of its species with Sonora followed by Durango (Table 4). This is particularly evident in amphibians, with over 80% of Chihuahuan amphibians shared with Sonora. For reptiles, Chihuahua shares nearly 77% of its species with Durango and 66% with Sonora. Chihuahua generally shares the least number of species with Coahuila, Sinaloa, and Texas. These patterns of shared species are likely a function of the extent to which these states share habitat types. For example, Chihuahua, Sonora, and Durango all have extensive desert habitats whereas Texas, for example, has a much more diverse range of habitats than Chihuahua. In addition, Sonora and Chihuahua share the habitats and species found in the Sierra Madre Occidental. Our results considering Chihuahua and all of its neighboring states parallels the results of an analysis of the states along the US-Mexico border using Jaccard hierarchical clustering analyses .

Conservation status
Most of the herpetofauna of Chihuahua falls in the IUCNs least concern category (119 of 132 [does not include DD species]; 90%), and as not listed by SEMARNAT (105 of 172; 61%) ( Table 2). These percentages are similar to those from other recently compiled tallies of conservation statuses for Mexican states (Coahuila: Lemos-Espinal and G. , Hidalgo: Lemos-Espinal and G. Smith 2015, Nayarit: Woolrich-Piña et al. 2016, Nuevo León: Lemos-Espinal et al. 2016. However, there are species of conservation concern in Chihuahua. For example, turtles and tortoises in Chihuahua appear to be a group of particular conservation concern with nearly half considered Vulnerable or Near Threatened by IUCN and more than half listed as Pr Table 4. Summary of the numbers of species shared between Chihuahua and neighboring Mexican and American states (not including introduced species). The percent of Chihuahuan species shared by a neighboring state are given in parentheses. Total refers to the total number of species found in Chihuahua and all the neighboring states (i.e., regional species pool) and the number in parentheses in this column is the percent of the regional species pool found in Chihuahua. --indicates either Chihuahua or the neighboring state has no species in the taxonomic group, thus no value for shared species is provided.   or A by SEMARNAT. Emydidae and Testudinae are the families of most conservation concern. Indeed, turtles account for 4 of the 13 species (31%) of the Chihuahuan herpetofauna that are categorized as Vulnerable, Near Threatened, or Endangered by the IUCN, even though they make up only 7% of the species in Chihuahua. We also found that turtles as a group also have the highest mean Environmental Vulnerability Score (EVS), especially Emydidae, Testudinidae, and Trionychidae. We therefore encourage additional emphasis be placed on better understanding the ecology and conservation status of turtle and tortoise populations in Chihuahua. In addition, even though there are relatively few reptiles and amphibians placed on conservation lists in Chihuahua, this does not mean they are safe. Indeed, there are species, such as Craugastor tarahumaraensis, Ctenosaura macrolopha, Uma paraphygas, and Tropidodipsas repleta that are of great conservation concern based on their EVS values (Wilson et al. 2013a, b). In addition, the more locally appropriate EVS assessments (see Wilson et al. 2013a,b) also suggest that conservation concern should exist for the amphibian families Ambystomatidae, Craugastoridae, and Eleutherodactylidae; and the non-turtle reptile families Anguidae, Eublepharidae, Iguanidae, Scincidae, Teiidae, and Elapidae.
Even beyond these species and families, the environment and habitats of Chihuahua are subject to anthropogenic change, such as construction of border fences (Lasky et al. 2011), increased urbanization (Biggs et al. 2010), and changes in precipitation and increased drying associated with climate change (Seager and Vecchi 2010). Indeed, the distribution of species at high risk according to the EVS assessment (≥ 14; Wilson et al. 2013a,b) is not the same across habitat types. Nearly 40% of species (18/47) in the temperate forests of the Sierra Madre Occidental is at risk according to the EVS, and nearly a third of species in the Chihuahuan Desert (19/58). Just over 20% (10/44) of species in subtropical canyons of the Sierra Madre Occidental are at high risk. Generalist species (those that use more than one habitat type) are the least at risk (2 of 25 species). These results suggest that particular conservation attention should be paid to the Sierra Madre Occidental and the Chihuahuan Desert habitat types in Chihuahua. We thus again emphasize that continued and increased study of the herpetofauna of Chihuahua is needed to monitor the possible effects of any environmental changes.