The state of Zacatecas is located in Mexico’s central northern region (Figure 1), representing 3.7 % of the country’s surface area. The altitude in the state ranges from 800 to 3,120 meters above sea level (INEGI 2017). The climate in the central region of the state is cold and semi-arid, whereas the climate in the northwestern region is hot and also semi-arid (INEGI 2008). Conversely, the climate in the northeastern portion of Zacatecas is hot and arid, with a mean annual temperature of 19 °C and an annual rainfall of 289 mm. Finally, the area filled with ravines towards the southwestern region of the state has a warm, Mediterranean-like climate during the summer. This is the bioclimatic region that most highly contrasts with the rest of the state (Climate Data 2018). This climate diversity results in four biogeographical provinces that meet within the state (Figure 2): Chihuahuan Desert province, Pacific Lowlands province and Sierra Madre Occidental province (Morrone et al. 2017).

Figure 1. 

Location of the state of Zacatecas and their climate types (modified from INEGI 2008).

Figure 2. 

Location of Zacatecas in central-northern Mexico and Physiographic Provinces in which this state is situated (map based on Morrone et al. 2017).

To determine the potential distribution of rattlesnakes in Zacatecas, we gathered records on their global presence. In order to do this, we conducted queries in the databases of the Global Biodiversity Information Facility: GBIF 2016; Vertebrate Networks: Vertnet 2016 and the National Commission for the Knowledge and Use of Biodiversity: CONABIO 2016. Specialized literature also provided presence records of Crotalus aquilus (Carbajal-Márquez et al. 2015a) and C. basiliscus in Zacatecas (Ahumada-Carrillo et al. 2011; Carbajal-Márquez et al. 2015b). Finally, we incorporated the presence records reported by Ávila-Herrera (2012), Ávila-Herrera et al. (2020), Esparza-Estrada (2014) Lara-Galván (2015) and our own field work. The total number of records was 12,113, which were subsequently reduced to 3,412 (Table 1) by eliminating duplicated, inaccurate or incomplete records. We also considered records containing complementary information, such as the location, species biology and information strictly referring to the site where organisms were observed in order to use that in the geo-referencing process. Of the total number of presence records used in the potential distribution models, 248 correspond to the state of Zacatecas.

According to Elith et al. (2011), when the study area or landscape of interest (L) is determined, it must contain a geographical area suggested and defined by the ecologist in relation to the problem, which can be delimited by geographical borders or by the knowledge of the point up to where the focal species may have spread. In addition, Merow et al. (2013) mentioned the importance of obtaining presence records for the species to be modeled, covering all the possible habitats where they might be found and the known distribution range of the species in question. Hence, the modelled presence records comprised the target species’ global distributions, and two different polygons that delimited the modelling extent. Thus, based on the IUCN (2020) classification for the species in the Crotalus genus reported in Zacatecas, two groups of study were established: 1) species endemic to Mexico and 2) species non-endemic to Mexico (Table 1). Based on this, the first polygon included the entire Mexican territory and was used to model the distribution of species endemic to Mexico (Crotalus aquilus, C. basiliscus and C. polystictus). The second polygon comprised the entire Mexican territory together with the southernmost states of the United States of America, namely, Arizona, Arkansas, California, Colorado, Kansas, Louisiana, Nevada, New Mexico, Oklahoma, Texas and Utah. This was done to include those species whose distribution range is also present in this portion of the USA (Crotalus atrox, C. lepidus, C. molossus, C. pricei, C. scutulatus and C. willardi).

We prepared distribution models using package sdm, version 1.0.46, implemented in the R software, which assembles and evaluates models using 15 algorithms: BIOCLIM, BIOCLIM.DISMO, BRT, CART, FDA, GAM, GLM, GLMNET, MARS, MAXENT, MAXLIKE, MDF, RF, RPART and SVM. This provides the potential distribution of a given species or community. For each species, we used all available presence points, in addition to several background points created randomly within the modelling extent, so that the proportion of presence points was 30 % for all species (Naimi and Araújo 2016).

We utilized a set of environmental variables that are typically associated with the presence of the species, the 19 bioclimatic variables from the WorldClim, version 2.0 database (Fick and Hijmans 2017). These data refer to the minimum, median and maximum temperature, as well as to the rainfall records from 1970 to 2000 and any deviations associated with these data. These variables have a spatial resolution of 30’’ or approximately 1 km². For the Mexican endemic species polygon, in addition to environmental variables, we included information on the land use, series V vegetation and edaphology (CONABIO 2017), rock types, topoform systems and the Mexican digital elevation continuum 3.0 (CEM 3.0). Further data was obtained from the National Statistics and Geography Institute (INEGI 2017), from which the slope and exposure were calculated. As for the non-endemic species polygon (Mexico and southern USA), we also included soil cover, human influence and the digital elevation continuum, downloaded from the Commission for Environmental Cooperation (CEC 2017), where the slope and exposure were also computed. Cartographic data was re-projected into the WGS_1984 world geographical coordinate system. The data of each predictor variable was cut out and retrieved. Map images were processed using ArcGIS 10.5 (ESRI 2016), QGIS 2.18.14 (QGIS 2009) and R 3.5.0 (R Core Team 2016).

Regarding variable selection (Table 2), we determined the most suitable variables for each species distribution model using the multGLM function in the fuzzySim R package (Barbosa 2015), where for each pair of correlated variables above |r| = 0.8, the function excludes the variable having the least significant relationship with the distribution of the species in question. The remaining variables are then subject to a stepwise selection process using the Akaike Information Criterion (AIC), to keep only informative variables in the models. Finally, any non-significant variables that might remain in the model after this process were eliminated (Reino et al. 2017; Gutiérrez-Rodríguez et al. 2017). The variables selected for each species were subsequently used to create models using the 15 algorithms applied in the sdm package. Afterwards, we calculated the mean and variance for each model’s predictions. The mean was used to show the potential distribution for each species of Crotalus, while the variance was used to estimate the agreement between predictions of different algorithms (Naimi and Araújo 2016). Finally, a potential distribution map was created based on the mean, cutting out the data to the surface of the region of interest, i.e. the state of Zacatecas.

Model evaluation was based on the criterion of area under the curve (AUC), which is considered a standard method to evaluate the discrimination capacity (i.e. differentiating the locations where presence and non-presence has been recorded) of predictive distribution models, avoiding the subjectivity of choosing a classification threshold. The value of AUC depends on the ratio of presence and the size of the area to be modeled, as pinpointed by (Lobo et al. 2008), but we used a constant prevalence value of 30 % for all species (Naimi and Araújo 2016).

To determine the rattlesnake number at the municipal level, we used the available presence records and prepared a list of the species observed at each municipality. Likewise, the list included the results of potential distribution models (Figures 3–11) that identified the areas bearing a higher suitability for these organisms. This implied overlapping the layer of municipalities over the potential distribution maps.

Figure 3. 

Presence and global potential distribution of Crotalus aquilus in Zacatecas, Mexico. Insert includes a C. aquilus from Tlachichila in the municipality of Nochistlán de Mejía (photo provided by Juan Felipe Martínez Montoya). The occurrence records used as input for the models are symbolized with dots, new records found during post-modeling field work are symbolized with triangles and the potential distribution is shown with warmer colors (red) identifying high potential for predicted presence for the species.

Based on the potential distribution models for each rattlesnake species found in Zacatecas, two localities per municipality were selected (three in the case of the Pinos, Loreto and Valparaíso municipalities). Thus, the field work in this study comprised a total of 48 localities throughout 22 municipalities within the state. These 22 municipalities were chosen randomly to include various regions throughout the state. Moreover, in these municipalities, we selected localities situated within the areas of greatest suitability as predicted by the models. A map of Mexican localities was overlapped to the potential distribution maps to conduct this geographical selection (CONABIO 2017). Field work was carried out in the areas surrounding the chosen localities in order to verify the presence of these species. To gather further information about these organisms, interviews were conducted to five individuals per locality, chosen randomly. Two of the five interviews targeted individuals who were believed to have closer contact with these organisms, i.e. individuals who engage in farming, cattle raising or rodent hunting. The other three interviews were carried out randomly, trying to include different age ranges and sexes. Finally, field verification was conducted in those areas having the most suitable habitats for the presence of these organisms based on the recommendations by Campbell and Lamar (2004), where the main criteria are related to land use, vegetation at elevation, including night driving along secondary roads, dirt roads and paths. At each location, we took into consideration visual records, skin sheds in good state, road kills and personal communications that could be confirmed (e.g. photographs and hunted specimens). A minimum sampling effort of 2 hours per location was considered, thus having a total of 243 hours of field work in a time period spanning from May to September of 2019, representing 22.09 field work hours/man.

In Zacatecas, the potential areas for the distribution of C. aquilus (Figure 3) are mainly found in the municipalities of Atolinga, Tepechitlán and Tlaltenango de Sánchez Román in the southwest. The distribution modeling also indicates areas in Genaro Codina, Cuauhtémoc and the municipality of Pinos, the latter in the southeastern region of the state. According to the distribution presented here, more organisms could be found in the border region between Aguascalientes and Zacatecas, since it presents a high degree of suitability for its occurrence, in addition to the municipalities of General Pánfilo Natera, Noria de Ángeles, Villa González Ortega and Villa Hidalgo that also present moderately high values. Regarding its global distribution, the largest number of records are located in the states of Guanajuato, Hidalgo and Querétaro, as well as specific records in Mexico City.

The western diamondback rattlesnake, Crotalus atrox is present in a large portion of the territory of Zacatecas (Figure 4), mainly along the northern region, which includes the municipalities of Concepción del Oro (where a record gathered during previous work is added), El Salvador and Mazapil. This species also showed records in the central and northern regions of the state, in the municipalities of Fresnillo and Río Grande, which exhibit distribution potential for the species. C. atrox has an extensive distribution in Zacatecas. During our post-modeling field work, many more individuals of this species were found in the municipalities of Concepción del Oro and Mazapil. The eastern region of Zacatecas has a low and medium suitability for this species, although a presence point is registered in the municipality of Chalchihuites. The southwestern region of Zacatecas stands out as the area having the lowest suitability throughout the entire state.

Figure 4. 

Presence and global potential distribution of Crotalus atrox in Zacatecas, Mexico. Insert includes a C. atrox from the municipality of Concepción del Oro (photo provided by Lenin Lara Galván). For explanation of the symbols and legend, see Figure 3.

The known distribution of C. basiliscus in Zacatecas is limited to the western and southwestern parts of the state (Figure 5). This species has presence records in the municipalities of El Plateado de Joaquín Amaro, Moyahua de Estrada and Valparaíso. However, the SDM indicates the following municipalities as medium suitability areas: Apozol, Atolinga, Jalpa, Juchipila, Mezquital del Oro, Momax, Monte Escobedo, Nochistlán de Mejía, Tepechitlán, Tlaltenango de Sánchez Román and Trinidad García de la Cadena. Two presence records were added by post-modelling field work, including a live specimen caught and released, which was provided by Bañuelos-Alamillo (pers. comm. 2018), as well as the record of a dead specimen provided by a resident from the locality of San Rafael de las Tablas. Both records are located within the municipality of Valparaíso and the zones in question are included in the delimited areas with the greatest distribution potential.

Figure 5. 

Presence and global potential distribution of Crotalus basiliscus in Zacatecas, Mexico. Insert includes a C. basiliscus from the municipality of Moyahua de Estrada (photo provided by Ivan Ahumada Carrillo). For explanation of the symbols and legend, see Figure 3.

The rock rattlesnake Crotalus lepidus is one of the species with most presence records in the state. The global potential distribution model for this species (Figure 6) contained a total of 375 occurrence records. Among these, 52 records are located in Zacatecas, mainly concentrating within the state’s central region, which is home to the largest urban areas and is composed of the municipalities of Guadalupe and Zacatecas. This species shows presence records primarily in the municipalities of Cuauhtémoc, Genaro Codina and Valparaíso. According to its global distribution model, its potential presence extends throughout the entire state of Zacatecas, from the municipalities of Pinos in the central region, where a significant number of records were identified, to the municipalities of Genaro Codina, Vetagrande and Villanueva. A few records were similarly identified in the northern region of the municipalities of Concepción del Oro, El Salvador, Cañitas de Felipe Pescador, General Francisco R. Murguía, Juan Aldama, Mazapil, Melchor Ocampo and Miguel Auza, in spite of showing a low suitability in the model. According to the SDM, the environment with the most suitable conditions for the presence of this species is located in the municipalities of Guadalupe, Jerez, Fresnillo, Monte Escobedo, Valparaíso, Vetagrande and Zacatecas. These rattlesnakes were found during post-modelling field work in the former two and the latter two municipalities. Two specimens were also spotted in the municipalities of Genaro Codina and Ojocaliente.

Figure 6. 

Presence and global potential distribution of Crotalus lepidus in Zacatecas, Mexico. Insert includes a C. lepidus from the semi-urban locality of Santa Monica in the municipality of Guadalupe (photo provided by Jesús Sigala Rodríguez). For explanation of the symbols and legend, see Figure 3.

The black-tailed rattlesnake (C. molossus) exhibits an extensive potential distribution within Zacatecas (Figure 7). This species spreads throughout the whole state, from the municipality of Pinos in the southeastern region to Sombrerete in the western region, with a substantial number of records along the northern region, particularly in the municipalities of Concepción del Oro and El Salvador. Specimens of this species were discovered in the municipalities of Guadalupe, Mazapil, Pánuco, Villanueva, Villa de Cos and Zacatecas during field work. One more organism and a clearly identifiable record of a skin shed of this species were found in Pinos. When inhabitants from different localities in some municipalities of Zacatecas were interviewed, they mentioned the black-tailed rattlesnake as the most abundant and most commonly observed species in parcels, dirt roads and paved roads. This species, together with C. atrox, are usually sold for food in the state capital. Conversely, Mezquital del Oro, Moyahua de Estrada and Trinidad García were some of the municipalities presenting a medium suitability for C. molossus, although the possibility of finding them in these areas cannot be ruled out.

Figure 7. 

Presence and global potential distribution of Crotalus molossus in Zacatecas, Mexico. Insert includes a C. molossus from the municipality of Pinos (photo provided by Lenin Lara Galván). For explanation of the symbols and legend, see Figure 3.

In the case of C. polystictus, the presence records (Figure 8) are concentrated in the western and southwestern region of the state, precisely in the municipalities Atolinga, Chalchihuites, El Plateado de Joaquín Amaro, Fresnillo, Jerez, Monte Escobedo, Sombrerete, Tabasco, Teúl de González Ortega and Valparaíso. Additional sources for Crotalus polystictus were consulted (Meik et al. 2012; Santiago-Pérez et al. 2017) to obtain a greater number of presence records. These zones also coincide with a high potential of suitability for their presence, according to the SDM. Besides, other regions of the municipalities of Apozol, Apulco, Juchipila, Tepechitlán and Genaro Codina were highlighted, the latter in the center-south of Zacatecas. On the other hand, the northern zone shows a low potential for its presence, so it is recommended to apply a greater sampling effort in the regions presented in red. In the central portion of the state, two new records for this species can be seen, which were provided by Bañuelos-Alamillo (2018). One is located in the municipality of Jerez and the other one in the nearby municipality of Valparaíso, both coinciding with an area of high suitability for C. polystictus.

Figure 8. 

Presence and global potential distribution of Crotalus polystictus in Zacatecas, Mexico. Insert includes a C. polystictus from the municipality of Atolina (photo provided by Iván Ahumada Carrillo). For explanation of the symbols and legend, see Figure 3.

Regarding its global distribution, it extends from Zacatecas to Mexico City and it is similarly reported in the states of Aguascalientes, Jalisco, Guanajuato, Michoacán, Querétaro and the State of Mexico, all of them exhibiting a significant number of records. In the southwestern portion of its known distribution, the record which is found closest to Colima was in the municipality of Tuxpan in Jalisco. Several authors mentioned that this species probably occurs Campbell and Lamar (2004) and is likely to occur Lemos-Espinal et al. (2020) in Colima. However, no presence records for this area were registered.

Unlike other species with a greater number of records, there were only two presence records of Crotalus pricei in Zacatecas, which are located in the municipalities of Genaro Codina and Villanueva. According to the SDM (Figure 9), the western region of Zacatecas presents the minimum essential ecological conditions for the presence of this species, mainly in the municipalities of Chalchihuites, the western portion of Fresnillo, Jerez, Jiménez del Teul, Monte Escobedo, the south of Sombrerete, Susticacán, the northern area of Tepetongo and especially the municipality of Valparaíso, which shows a high potential for its development. On the other hand, in the northern region of Zacatecas, these parameters were found in Concepción del Oro, El Salvador and Mazapil, which could be due to the occurrence records in the northeast region of its global distribution. This extends from Arizona in the southern United States, down to Mexico throughout the states of Sonora, Chihuahua and Durango, with the latter two being the states where the largest number of C. pricei records were concentrated, together with those located in the state of Nuevo León. In the center of Mexico, it is possible to find two specific records in San Luis Potosí, one mentioned by Grünwald et al. (2012) and an additional one included in the personal field work database of Jesús Sigala.

Figure 9. 

Presence and global potential distribution of Crotalus pricei in Zacatecas, Mexico. Insert includes a C. pricei from Durango state (photo provided by Jesús Sigala Rodríguez). For explanation of the symbols and legend, see Figure 3.

During the field work, no direct observations or skin sheddings were identified for this species, although there are two records a few kilometers from the Zacatecas border. One of them is located in the municipality of Mezquitic, Durango (Grünwald et al. 2012) and a more recent one is situated in Mezquital, also in the state of Durango, and included in the personal database of Jesús Sigala. In Zacatecas, this species can be considered rare, which evidences the necessity for increased field work efforts, especially at high altitudes, since the records hereby presented were found in areas > 2,500 m., thus lying within the altitude range reported by Campbell and Lamar (2004), precisely 1,850 – 3,203 m. Therefore, it is recommended to sample high elevation areas that coincide with the greatest potential for the distribution of this species in order to confirm its presence, as well as to increase the number of records and carry out a modeling based on the presence of this organism.

Crotalus scutulatus is one of the species with the greatest number of records for the construction of the SDM (Figure 10). The points of occurrence gathered are mainly located in the municipalities of Guadalupe and Zacatecas, spreading their distribution range both northwards into the municipalities of General Francisco R. Murguía, Fresnillo, Río Grande and Sain Alto, and southwards, starting from Ojocaliente and finishing in Pinos. Valparaíso concentrates a substantial amount of records for this species, which is also found on the other side of the state, namely, in the municipality of Concepción del Oro. During field work, this species was identified in the municipality of Pánfilo Natera in an area of abundant plateaus and barren soil. C. scutulatus is essentially present throughout the entire state, although the southern and southwestern regions have a medium potential suitability.

Figure 10. 

Presence and global potential distribution of Crotalus scutulatus in Zacatecas, Mexico. Insert includes a C. scutulatus from Pedregoso in the municipality of Pinos (photo provided by Lenin Lara Galván). For explanation of the symbols and legend, see Figure 3.

Finally, the occurrence data and the potential distribution map of C. willardi are shown in Figure 11. To prepare the modelling of this species throughout its known distribution range, 84 geo-referenced points were available. Among these, two were registered in Sombrerete and one in Valparaíso and according to the SDM, they are also the municipalities of Zacatecas that exhibit the greatest potential for their distribution. In addition, specific areas with high potential for its presence are shown in Fresnillo, Jiménez del Teul, Monte Escobedo and a series of municipalities in the southwestern region of the state. Along with C. pricei, this is one of the species with the lowest number of occurrence records in Zacatecas. Regarding their global distribution, the presence records are spread in the western region of Mexico, mainly in the states of Durango, Chihuahua and Sonora, as well as in Arizona and New Mexico in the United States. It is recommended to apply greater sampling efforts in Valparaíso and Sombrerete, especially in the Durango-Zacatecas border area in order to increase the number of localities for this species in the region.

Figure 11. 

Presence and global potential distribution of Crotalus willardi in Zacatecas, Mexico. Insert includes a C. willardi from the state of Durango (photo provided by Joseph E. Forks). For explanation of the symbols and legend, see Figure 3.

Thirty-nine (67.24 %) out of the fifty-eight municipalities (Table 3) have at least one record of rattlesnake species. During the field verification performed in the potential distribution areas for these organisms in Zacatecas, twenty-seven new occurrence records belonging to six species (Crotalus atrox, C. basiliscus, C. lepidus, C. molossus, C. polysticus and C. scutulatus) and one more unpublished record for C. aquilus were added. According to the compilation of total records, Sombrerete and Valparaíso were the municipalities exhibiting the highest rattlesnake diversity, with six different species being reported, followed by Fresnillo, with five different species. The municipalities of Chalchihuites, Concepción del Oro, El Plateado de Joaquín Amaro, Genaro Codina, Guadalupe, Mazapil, Monte Escobedo and Pinos reported four species each. The municipality of Zacatecas, where the state capital is located, has the presence of three species of this genus. Although there are no occurrence records for rattlesnakes in 19 municipalities, according to the SDM, all municipalities have the minimum conditions for the presence of rattlesnakes. It is noteworthy that C. molossus has reported presence in 24 municipalities and C. lepidus and C. scutulatus in 23 municipalities, as opposed to C. pricei and C. willardi, reported in only two municipalities.