A conservation checklist of the amphibians and reptiles of Sonora, Mexico, with updated species lists

Abstract Sonora has a rich natural diversity, including reptiles and amphibians. Sonora’s location on the United States-Mexico border creates some unique conservation challenges for its wildlife. We compiled a list of the amphibian and reptile species currently known for Sonora, summarized the conservation status of these species, and compared our list of species with known species lists for adjacent states. The herpetofauna of Sonora comprises 200 species of amphibians and reptiles (38 amphibians and 162 reptiles). Overall, Sonora shares the most species with Chihuahua, Sinaloa, and Arizona. Approximately 11% of the amphibian and reptile species are IUCN listed, but 35.5% are placed in a protected category by SEMARNAT, and 32.6% are categorized as high risk by the Environmental Vulnerability Score.


Introduction
Sonora is a state that, due to its geographic location near the U.S. states of Arizona and California and the extraordinary natural diversity those states host, has attracted the attention of specialists and amateurs in the study of its flora and fauna. Therefore, Sonora's biodiversity is perhaps the best known among the states of northern Mexico. fers for human use (Contreras-B. andLozano-V. 1994, Halvorson et al. 2003). Climate change is also likely to increase the strain on freshwater aquifers in Sonora (Scott et al. 2012) and the region encompassing the US-Mexico border areas (Ye and Grimm 2013).
The factors mentioned above are likely to affect several taxonomic groups, but the herpetofauna is a group of particular concern. Rorabaugh (2008) found that 40% of the Sonoran herpetofauna were given some conservation status by the Mexican government (SEMARNAT) or the IUCN Red List. Although there have been several recent works that report lists of species of reptiles and amphibians in Sonora (Rorabaugh 2008, Enderson et al. 2009, Lemos-Espinal and Smith 2009, Lemos-Espinal and Rorabaugh 2015, Rorabaugh and Lemos-Espinal 2016, species additions and accelerating taxonomic changes merit a new analysis of the current list for Sonora, especially with respect to the conservation status of the species listed. Here, Figure 2. Climate map of the state of Sonora, Mexico (modified from García -CONABIO 1998). we report the list of species currently known for the state of Sonora, focusing on the conservation status reported for each species, analyzing it by taxonomic groups and ecoregions, and comparing our list of species with known lists for adjacent states.

Methods
We only included species in the checklist for which we could confirm the record in Sonora, either by direct observation or through documented museum records or vouchers. We follow Frost (2018) or AmphibiaWeb (2018) for amphibian names and Uetz and Hošek (2018) for reptile names (for a summary of recent taxonomic changes see Table 1). We compiled the list of amphibians and reptiles of the state of Sonora from the following sources: (1) our own field work; (2) specimens from the Amphibians and Reptiles collection of the University of Arizona; (3) specimens from the Laboratorio de Ecología -UBIPRO (LEUBIPRO) collections; (4) a thorough examination of the available literature on amphibians and reptiles in the state; (5) amphibian and reptile records for the state of Sonora in VertNet.org; and (6) databases from the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO, or National Commission for the Understanding and Use of Biodiversity) (see Appendix 1).
We recognize six herpetological ecoregions in Sonora (Eastern Mountains, High Northeastern Valleys, Western Mainland Deserts, Subtropical Lowlands and Foothills of the Sierra Madre Occidental, Islands, and Marine), each of which supports distinctive amphibian and reptile assemblages (Fig. 3). These ecoregions are further defined by geography, elevational range, topography, and vegetation communities (see Lemos-Espinal and Rorabaugh 2015;Rorabaugh and Lemos-Espinal 2016 for a description of these ecoregions). As a result, boundaries of ecoregions bear some resemblance to those of physiographic units (Fig. 4) and vegetation communities (Fig. 5).
We recorded the conservation status of each species based on 1) the IUCN Red List 2018-2; 2) Environmental Viability Scores from Wilson et al. (2013a, b); and 3) listing in Table 1. Recent taxonomic changes for the herpetofauna of Sonora.

Taxon Explanation
Rhinella horribilis Acevedo et al. (2016) demonstrated that there were two separate evolutionary lineages within Rhinella marina representing two distinct species: R. marina for the eastern populations, and R. horribilis for the western populations.
Rana Frost et al. (2006) recommended the use of the name Lithobates for North American Rana. However, we use Rana because Yuan et al. (2016) recently returned all Lithobates to 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.

Isthmura sierraoccidentalis
Originally Isthmura sierraoccidentalis was described as a subspecies of Pseudoeurycea belli by Lowe et al. (1968), recently it was elevated to full species status by Rovito et al. (2015).
Aspidoscelis Tucker et al. (2016), based on Steyskal (1971), explained and justified why the genus name Aspidoscelis should be treated as masculine, thus we use the appropriate masculine species names.
Boa Card et al. (2016) recently recognized the Boa populations from the slopes of the Mexican Pacific as Boa sigma, which we follow. Chionactis annulata Wood et al. (2014) raised Chionactis occipitalis annulata to full species status (C. annulata).
Chionactis, Chilomeniscus, and Sonora Cox et al. (2018) concluded that Sonora is paraphyletic with respect to Chilomeniscus and Chionactis and found additional evidence to suggest synonomizing Chionactis and Chilomeniscus with Sonora. However, due to the long history of the use of the names of these three genera, we retain the use of the three genera to reduce confusion. In addition, other interpretations of the work of Cox et al. (2018) leave the current arrangement in place instead of synonymizing them (A Holycross and D Wood pers. comm.).

Lampropeltis
Based on the work of Krysko et al. (2017) the state of Sonora hosts three species of the Lampropeltis getula complex: Lampropeltis californiae along most of the border with Arizona; Lampropeltis splendida in the northeastern corner of the state, in the region where Arizona, New Mexico, Chihuahua and Sonora converge; and Lampropeltis nigrita, occupying most of the state of Sonora, including the islands of Tiburón and San Pedro Nolasco. Meik et al. (2015) elevated Crotalus mitchelli pyrrhus to full species status, so we report C. pyrrhus as occurring in Sonora.   [Baird & Girard] for L. getula Linnaeus [Krysko et al. 2017]). We created species accumulation curves for the total herpetofauna, amphibians, and reptiles using the year of the first recorded observation for each species. Such species accumulation curves are likely to be reasonable estimates of the species richness of amphibians and reptiles (see Raxworthy et al. 2012).

Results and discussion
Sonora hosts a total of 200 (seven of them introduced) species of amphibians and reptiles. This is an increase of four species from the list compiled by Rorabaugh and Lemos-Espinal (2016), and 13 species from the list compiled by Enderson et al. (2009) The species accumulation curves for all species, amphibians only, and reptiles only suggest that the current list of species likely underestimates the species richness for Sonora (Fig. 6). These curves show a rapid increase in species during the first half of the 20 th century with a steady, almost linear, increase in the number of species recorded in Sonora. Following a brief period of little additional accumulation of new species recorded in Sonora in the late 1900's, there has been a recent increase in the number of species added to the Sonoran herpetofauna. This increase includes recent documentation of non-native species (Apalone spinifera, Hemidactylus frenatus, and H. turcicus), as well as recent taxonomic changes (see Table 1).
We compiled a list of 17 species (three amphibians, 14 reptiles) potentially occurring in Sonora (Table 4) based on species for which undocumented observations in Sonora exist but for which museum or other records are not available, and on species that have not been recorded or observed in the state, but whose distributional ranges come close to the borders of Sonora. We did not include these species in our analyses and summaries.

General distribution
Fourteen of the 38 species of amphibians that inhabit Sonora are endemic to Mexico, one of which is restricted to small areas in the Sierra Madre Occidental in eastern Sonora and western Chihuahua (Table 2). Four more are distributed in the Sierra Madre Occidental mainly in the states of Chihuahua, Durango, Sinaloa, and Sonora (Table 2). Another six species are distributed along the Pacific coast, and three more along the Pacific coast extending eastward through the Balsas depression, with one of these three even reaching the state of Veracruz (Table 2). Of the 24 amphibian species not endemic to Mexico that inhabit Sonora, two are introduced species, 17 more are found in the US and Mexico, and the remaining five species have a wide distribution Table 2. Amphibians and reptiles of Sonora with distributional and conservation status. Ecoregion (1 = Western mainland deserts; 2 = High northeastern valleys; 3 = Eastern mountains; 4 = Subtropical lowlands and foothills; 5 = Marine; 6 = Islands); IUCN Status (DD = Data Deficient; LC = Least Concern, VU = Vulnerable, NT = Near Threatened; EN = Endangered; CE = Critically Endangered; NE = not Evaluated) according to the IUCN Red List (The IUCN Red List of Threatened Species, Version 2018-1; www. iucnredlist.org; accessed 14 September 2018), conservation status in Mexico according to SEMARNAT (2010) (P = in danger of extinction, A = threatened; Pr = subject to special protection, NL -not listed), and Environmental Vulnerability Score (EVS -the higher the score the greater the vulnerability: low (L) vulnerability species (EVS of 3-9); medium (M) vulnerability species (EVS of 10-13); and high (H) vulnerability species (EVS of 14-20) from Wilson et al. (2013a,b) and Johnson et al. (2015). Global Distribution (GD): 0 = Endemic to Sonora; 1 = Endemic to Mexico; 2 = Shared between the US and Mexico; 3 = widely distributed from Canada or the US to Central or South America; 4 = widely distributed from Mexico to Central America; 5 = circumglobal distribution; 6 = Pacific and Indian Oceans; IN = Introduced to Sonora. Source of first record (year in parentheses) is the voucher specimen (see Appendix 1 for abbreviations) or paper associated with the first documentation of a species in Sonora.   Table 2 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) and conservation status in Mexico according to SEMARNAT (2010) in the order NL, Pr, A, and P (see Table 1 for abbreviations). Mean EVS is the mean Environmental Vulnerability Score, scores ≥ 14 are considered high vulnerability (Wilson et al. 2013a, b). from Canada to Central America, from the US to Central or South America, or from Mexico to Central or South America ( Table 2). The American Crocodile (Crocodylus acutus) is widely distributed from the eastern US to South America. One of the seventeen species of turtles that inhabit the state is endemic to Sonora (Table 2). Five more are endemic to Mexico. Of the eleven species of turtles not endemic to Mexico that occur in Sonora, one is introduced. Four more are distributed from the US to Mexico, one more is found from Mexico to Central America, and the remaining five species have a circumtropical or circumglobal distribution ( Table  2). Fourteen of the 69 species of lizards that occur in the state are endemic to Sonora, nine of them to islands of the Gulf of California. Thirteen more are endemic to Mexico (Table 2). Of the 42 lizard species not endemic to Mexico that inhabit Sonora, three are introduced, 38 more are found in the US and Mexico, and the remaining species have a wide distribution that includes Mexico and South America (Phyllodactylus tuberculosus) ( Table 2). Two of the 75 species of snakes that inhabit the state are endemic to Sonoran islands of the Gulf of California (Table 2). Another 21 snake species that are found in Sonora are endemic to Mexico. Of the 52 snake species not endemic to Mexico that occur in Sonora, one is introduced, 41 more are distributed from the US to Mexico, six more range from the US or Canada to Central or even South America, and three more are found from Mexico to Central or South America (Table 2).

Ecoregions
The most diverse Sonora ecoregions in terms of the herpetofauna are the Eastern mountains (54% of the total number of amphibian and reptile species for the state) represented by the Sierra Madre Occidental and associated mountains, and the Western Mainland Desert (49%) represented mainly by the Sonoran Desert (Fig.  4). The Island (16%) and Marine (4%) are the least occupied ecoregions (Table 5). In general, the highest richness of amphibian species is observed in the Subtropical Lowlands and Foothills of the Sierra Madre Occidental with 61% of the total number of species, followed by the Eastern Mountains (58%), the Western Mainland Deserts (50%), and the High Northeastern Valleys (39%). Amphibians are almost absent in the Island ecoregion with only two species recorded (6%) and due to their limitations to inhabit saline environments they are absent in the Marine ecoregion ( Table 5). The Subtropical Lowlands and Foothills of the Sierra Madre Occidental had 67% of the anuran species in Sonora, whereas caudate amphibians are absent in this ecoregion showing their highest percentage of presence in the Eastern Mountains with two (67%) of the three species occurring in this ecoregion. In reptiles, the highest species richness is found in the Eastern Mountains (53%) ecoregion. This is the ecoregion with the highest number of snake (61%) and turtle (44%) species, although the same number of turtle species is found in the Subtropical Lowlands and Foothills of the Sierra Madre Occidental. Snakes are also diverse in the Western Mainland Deserts and the Subtropical Lowlands and Foothills of the Sierra Madre Occidental; each of these ecoregions hosts 38 snake species (51% of the total number of snake species recorded in Sonora). On the other hand, due to their conspicuousness and adaptations for arid environments, lizards have their highest diversity in the Western Mainland Deserts (48%) followed by the Eastern Mountains (47%), and they are the most diverse taxonomic group in the Island ecoregion, which is represented by dry environments, with 15 species (23%). Snakes are also diverse in the Island ecoregion with 13 species (18%). This is explained in part by the high vagility, adaptations to dry environments, and speciation rates of these two squamate suborders. Testudines is the taxonomic group with the highest percentage of species (5 = 31% of the total number of turtles in Sonora) in the Marine ecoregion, followed by snakes and crocodilians, both groups with one species representing 1 and 100% of the total number of species in their groups respectively. Five of the species that occur in the Marine ecoregion have a circumglobal or circumtropical distribution (five turtles). The other two species occurring in the Marine ecoregion are a crocodile that was thought until recently to be extirpated from Sonora but may be staging a comeback on the southern coast (Rorabaugh 2017), and a sea snake distributed across the Pacific and Indo-Pacific Oceans. The general reptile pattern of diversity is driven by lizards and snakes, except in the Marine ecoregions which is dominated by sea turtles of the families Cheloniidae and Dermochelyidae (Table 5). Table 4. List of amphibians and reptiles that could potentially occur in Sonora.

Class Amphibia Order Anura Craugastoridae
Craugastor vocalis (Taylor, 1940) Likely to occur in tropical deciduous forest and montane woodlands in the Río Fuerte drainage of extreme southeastern Sonora.

Ranidae
Rana blairi (Mecham, Littlejohn,Oldham, Brown, & Brown, 1973) Likely to occur in Chihuahuan Desert or semi-desert grassland of northeastern Sonora, along the US-Mexico border east of Naco.

Scaphiopodidae
Spea bombifrons (Cope, 1863) Likely to occur in Chihuahua desertscrub east and plains grassland of northeastern Sonora.

Class Reptilia Order Squamata Suborder Amphisbaenia
Bipes biporus (Cope, 1894) This species has been observed in the San Carlos Bay, municipality of Guaymas (Ballinger pers. comm., May 2009), but no museum record or voucher exist to support its presence in Sonora.

Suborder Lacertilia Anguidae
Barisia levicolis (Smith, 1942) Likely to occur in woodlands of the Sierra Madre Occidental of eastern and northeastern Sonora Phrynosomatidae & Brattstrom, 1955 Expected in Chihuahuan desertscrub and semi-desert grassland valleys as well as the lower slopes of the mountains along the US -Mexico border from the Río San Pedro valley east to the Sierra San Luis, and potentially in Plains grassland in the southern Animas Valley (northeastern Sonora). Scincidae Plestiodon multilineatus (Tanner, 1957) Likely to occur in woodland of the Sierra Madre Occidental of eastern and northeastern Sonora Suborder Serpentes Boidae Lichanura orcutti Stejneger, 1889 Has been found within a few km of the Sonora border in the Tinajas Altas Mountains of Yuma County, Arizona Colubridae Lampropeltis gentilis (Baird & Girard, 1853) Occurs in southeastern Cochise County, Arizona

Tantilla nigriceps Kennicott, 1860
Likely occurs in northeastern Sonora in Chihuahuan desertscrub or semi-desert grassland from Agua Prieta east to the Sierra San Luis and possibly in Plains grassland in the southern Animas Valley. Dipsadidae Hypsiglena jani Duges, 1865 Likely to occur in tropical deciduous forest and scrubland of southeastern Sonora. Hypsiglena torquata (Günther, 1860) Likely to occur in tropical deciduous forest and scrubland of southeastern Sonora. Mulcahy et al. (2014) suggested the snakes in this area might be an undescribed species of Hypsiglena. Rhadinaea laureata (Günther, 1868) Likely to occur in woodlands of the Sierra Madre Occidental of eastern and northeastern Sonora Leptotyphlopidae Rena dissecta (Cope, 1896) Expected in Chihuahuan desertscrub, semi-desert grasslands, and into the lower slopes of adjacent mountains along the United States -Mexico border from the Río San Pedro Valley east to the Sierra San Luis, and also in Plains grassland in the southern Animas Valley. Natricidae Thamnophis elegans (Baird & Girard, 1853) This species might occur in the Sierras Huachinera and Bacadehuachi and possibly elsewhere in the eastern mountains of Sonora near the Chihuahua border. Viperidae Sistrurus tergeminus (Say, 1823) Could potentially be found in grasslands along the US -Mexico border from the Río San Pedro Valley east to the Sierra San Luis.

Order Testudines Emydidae
Trachemys scripta (Thunberg, 1792) This aquatic turtle occurs sparingly as an introduced species in the Colorado River near Yuma, Arizona and in the San Pedro River Valley of Arizona. It could be present along wetted reaches of the Río Colorado in Sonora or in agricultural canals and ditches in that region, and in the Río San Pedro of Sonora near the border with Arizona.

Comparisons with neighboring states
Overall, Sonora shares the most species with Chihuahua, Sinaloa, and Arizona (Table 6). For amphibians, Sonora shares the most species with Chihuahua and Sinaloa. For reptiles, Sonora shares about half its species with Chihuahua, Sinaloa, and Arizona (Table 6). Previous comparisons of shared herpetofaunal species among neighboring states in the US-Mexico border region found high levels of similarity between Sonora and Chihuahua (Enderson et al. 2009, Lemos-Espinal et al. 2017. However, an analysis based on "biogeographic affinity" resulted in Sonora being closest or most similar to Sinaloa (Enderson et al. 2009, Lavín-Murcio andLazcano 2010). There is some variation, though, in these affinities depending on which specific herpetofaunal taxa are being examined (Enderson et al. 2009). Such a pattern probably reflects the fact that Sonora, Chihuahua, Arizona, and Sinaloa all have extensive tracts of arid habitats. Shared habitats and vegetation types likely lead to similarities in species among Sonora and neighboring states (see also Smith and Lemos-Espinal 2015, Lemos-Espinal and Smith 2016, Lemos-Espinal et al. 2017. The similarity in herpetofauna among three Mexican states and Arizona highlights the necessity for interstate and international approaches to conserving and managing habitats and species (e.g., Grigione et al. 2009, Wiederholt et al. 2013.

Conservation status
A total of 21 (= 10.9%) species of amphibians and reptiles is IUCN listed (i.e., Vulnerable, Near Threatened, Endangered, or Critically Endangered), but 69 species (= 35.0%) are placed in a protected category by SEMARNAT and 63 species (= 32.6%) are categorized as high risk by the EVS (Tables 3, 5). For amphibians, 11.1% are IUCN  (Tables 3, 5). These results suggest that the herpetofauna, especially the reptiles, of Sonora is considered to be of relatively low conservation concern at a global scale, but there is much greater conservation concern at a national level. Indeed, more local assessments (SEMARNAT and EVS) are based on information specific to Mexico and thus are more likely to reflect the conservation needs of the Sonoran herpetofauna (see Lemos-Espinal et al. 2018a,b for a similar assessment for other Mexican states). 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 Bufonidae, Craugastoridae, Eleutherodactylidae, Ranidae, Ambystomidae, Crocodylidae, Helodermatidae, Iguanidae, Phrynosomatidae, Phyllodactylidae, Teiidae, Xantusidae, Colubridae, Dipsadidae, Elapidae, Natricidae, Viperidae, Cheloniidae, Dermochelyidae, Emydidae, Kinosternidae, and Testudinidae (Tables 3, 5). Because the IUCN, SEMARNAT, and EVS categories are based on global or country-level assessments, there are likely amphibians and reptiles whose conservation status in Sonora is not accurately assessed by these measures. Additional assessments at the state level in Sonora, and other Mexican states, are needed to establish conservation or management needs for particular states, or even regions. As an example, frogs in the family Ranidae in Sonora, some of which are considered of conservation concern, are at risk from habitat loss, disease (chytridiomycosis), and predation by introduced species (Rorabaugh and Lemos-Espinal 2016).
To help determine which ecoregions within Sonora support species of particular conservation concern, we summarized the conservation status of reptile and amphibian taxa in each ecoregion found in Sonora (Tables 2, 3). In regard to IUCN categories, none of the amphibians in the Western Mainland Deserts, Subtropical Lowlands and Foothills of the Sierra Madre Occidental, and Island ecoregions are listed; however, one species (2.8%) in the High Northeastern Valleys, and three (8.3%) in the Eastern Mountains ecoregions are included. For SEMARNAT categories, 16.7% of amphibians in the Western Mainland Deserts ecoregion, 14.3% in the High Northeastern Valleys ecoregion, 28.6% in the Eastern Mountains ecoregion, and 18.2% in the Subtropical Lowlands and Foothills of the Sierra Madre Occidental ecoregion are listed. For EVS, 44.4% of the amphibians in the Western Mainland Deserts ecoregion were in the low and medium categories, and 5.6%, represented by only one species, was in the high category; the remaining 5.6% are represented by a species not evaluated. More than half (57.1%) of the amphibians in the High Northeastern Valleys ecoregion are in the low category, and 42.9% are in the medium category; no species in this ecoregion is in the high category. In the Eastern Mountains ecoregion, 38.1% of amphibian species are in the low and medium categories, 19.0% in the high, and the remaining 4.8% are represented by a species not evaluated. For the Subtropical Lowlands and Foothills of the Sierra Madre Occidental ecoregion, 50.0% are in the low category, 36.4% are in the medium category, and 9.1% are in the high category; the remaining 4.5% are represented by a species not evaluated. For the Island ecoregion, the two species occurring in this ecoregion are in the low category.
For the IUCN listings, all ecoregions, except the Marine ecoregion, have relatively few species of reptiles in the protected categories (Western Mainland Deserts [5 = 6.6%], High Northeastern Valleys [3 = 7.5%], Eastern Mountains [6 = 7.2%], Subtropical Lowlands and Foothills of the Sierra Madre Occidental [4 = 6.6%], and Island [3 = 10.5%]). Nearly all of the reptiles in the Marine ecoregion (6 = 85.7%) are in the protected categories. However, for the IUCN listing a total of 38 reptile species have not been evaluated, most of them are species recently described or not recognized by the IUCN as populations that deserve species status, but all of them are species with a narrow distribution, which increases their vulnerability. On the other hand, 36.8% of reptiles in the Western Mainland Deserts region, 42.5% from the High Northeastern Valleys ecoregion, 35.4% from the Eastern Mountains ecoregion, 37.1% from the Subtropical Lowlands and Foothills of the Sierra Madre Occidental ecoregion, 85.7% of the Marine ecoregion, and 41.4% from the Island ecoregion are in the protected SEMARNAT categories. For the Western Mainland Deserts ecoregion, 26.3% of the reptiles are in the low EVS category, 36.8% in the medium, and 32.9% in the high; the remaining 3.9% are represented by three species not evaluated. In the High Northeastern Valleys ecoregion, 27.5% of the reptiles are in the low, 47.5% in the medium, and 22.5% in the high category; the remaining 2.5% are represented by a species not evaluated. Of the reptiles in the Eastern Mountains ecoregion, 19.5% are in the low, 39.0% in the medium, and 35.4% in the high category; the remaining 6.1% are represented by five species not evaluated. For the Subtropical Lowlands and Foothills of the Sierra Madre Occidental, 27.4% are in the low EVS category, 32.3% in the medium, and 33.9% in the high; the remaining 6.5% are represented by four species not evaluated. Of the seven reptile species that occur in the Marine ecoregion, only one (14.3%) is in the high category; the other six species (85.7%) are species that have not been evaluated. In the Island ecoregion, 17.2% are in the low EVS category, 24.1% in the medium, and 48.3% in the high; the remaining 10.3% are represented by three species not evaluated. Thus, the reptiles in the Marine ecoregion are clearly the most threatened of the Sonoran herpetofauna.