Altitudinal Adaptation of Crotalus Intermedius Troschel, 1865 in a Natural Protected Area from Mexico (Squamata: Viperidae)

Herpetology Notes, volume 13: 883-889 (2020) (published online on 22 October 2020)

Altitudinal adaptation of Crotalus intermedius Troschel, 1865 in a natural protected area from Mexico (Squamata: Viperidae)

Ricardo Serna-Lagunes1,*, Gerardo B. Torres-Cantú1, Pablo Andrés-Meza1, Norma Mora-Collado1, Régulo Carlos Llarena-Hernández1, and Otto Raúl Leyva-Ovalle1

The Mexican small-headed rattlesnake, Crotalus Reptiles depend on the selection of an appropriate intermedius Troschel, 1865, is a venomous pit viper thermal microhabitat to acquire and maintain the species endemic to Mexico, distributed in disjunct optimum body temperature for proper physiological populations (McCranie, 1991) in the Trans-Mexican function (Angilletta, 2001). As environmental Volcanic Belt region and southern Mexican Highlands, temperature presents a negative correlation with where the states of Hidalgo, Puebla, western Veracruz, altitude, this correlation may delimit the geographical northeast of the State of Mexico and Tlaxcala, southeast distribution of viperids (Huang et al., 2007; Seok et al., of Morelos, eastern Guerrero and northern Oaxaca 2017) and its variation may favour the colonisation of converge (Campbell and Lamar, 1989; McCranie, 1991; new locations by some individuals of C. intermedius, Correa-Cano et al., 2009; Paredes-García et al., 2011; making it possible to record the species in areas without Aldape-López and Santos-Moreno, 2016; Fernández- previous records or outside its potential distribution Badillo et al., 2016). The species occurs mainly in (Fernández-Badillo et al., 2016). natural protected areas (Canseco-Márquez et al., 2007) Pico de Orizaba is the largest mountain in Mexico with low populational abundance (Bryson et al., 2011), and the PONP protects mountain ecosystems such as its type locality is undetermined (McCranie, 1991) and coniferous forests and mesophilic mountain forests. its conservation status is considered as “threatened” In recent years, variations in the temperature and (SEMARNAT, 2010). precipitation pattern associated with the phenomenon There are records of geographic distribution of C. of global climate change have been registered in the intermedius in vegetation such as the xerophilous scrub PONP (Caballero et al., 2010; Manzanilla-Quiñones et (Valencia-Hernández et al., 2007), oak scrub, pine-oak al., 2018). This may promote/limit the colonisation of forest, could mountain forest and deserts (Hernández- C. intermedius towards higher altitude habitats because Jandete et al., 2017). The species is reported between of its adaptive capacity (Urbina-Cardona, 2016), but to 2,000 and 3,200 m a.s.l. (Campbell and Lamar, 1989, date, the altitudinal distribution threshold for this specie 2004; Fernández-Badillo et al., 2016), but its range in the PONP has not been documented. The objective of distribution in the Pico de Orizaba National Park of this work is to describe the potential distribution (PONP) has not yet been recorded, which would be and document the altitudinal variation in records of useful to identify priority areas to channel efforts for its the Mexican small-headed rattlesnake, C. intermedius, management and protection. in the PONP, Mexico. The information generated represents the description of a fraction of the ecological niche of C. intermedius in the PONP that can be used to direct conservation efforts towards areas suitable for the survival of the species. The present study was conducted in the PONP located in the states of Veracruz and Puebla (19.0503°N, 1 Laboratorio de Bioinformática y Bioestadística. Facultad 97.2196°W and 19.0497°N, 97.2183°W, respectively; de Ciencias Biológicas y Agropecuarias, región Orizaba- Córdoba, Universidad Veracruzana, Peñuela, S/N, Col. Datum WGS 84; Fig. 1). Its maximum altitude is 5,636 Centro, Amatlán de los Reyes, Veracruz 94945, México. m a.s.l. with a mild-humid climate, and precipitation * Corresponding author. E-mail: [email protected] and temperature annual averages are 1,698 mm and 884 Ricardo Serna-Lagunes et al.

al., 2018). Prior to the analysis, to eliminate repeated occurrences, atypical coordinates or coordinate errors, a quality analysis of georeferenced sampling points was applied with the Google Fusion Table Tool (López- Collado, 2020). Using the ArcGis software version 10, the geographic coordinates of the species presence were plotted on the three environmental variables layers used in the model (precipitation [mm], temperature [°C], and evaporation [mm]) and one geographical variable (altitude [m a.s.l.]). With the point value extraction tool, the average values of each variable were obtained (Tables 1–2). These variables were chosen since they determine the range of geographic distribution of reptiles (Urbina-Cardona and Flores-Villela, 2010; Boyle et al., 2016). In this study, we did not apply a correlation test for each pair of environmental variables used in the model because the variables were chosen based on the biological knowledge of the species, which provides a more realistic prediction of the distribution in the cross-time (Guevara-López et al., 2018). The variables (precipitation, temperature, evaporation, and altitude) were obtained from the Digital Climate Atlas of Mexico to a resolution of 926 m (Fernández-Eguiarte et al., Figure 1. Potential distribution model of Crotalus intermedius 2012), were adjusted for the polygon that comprises the in the Pico de Orizaba National Park (PONP), in Mexico and PONP, and were used as “background” to develop the black circles represent the new records for the expansion of its species distribution model using the MaxEnt software distribution for the validation of the field model. version 3.4 (Phillips et al., 2006; Phillips and Dudik, 2008). The distribution model was constructed using 30% of the occurrences as a percentage of random evaluation of 9.3° C, respectively (García, 1988). The predominant model and 70% for model construction. Extrapolation vegetation corresponds to pine forest (Pinus hartwegii), option and “do clamping” were deactivated to avoid pine-oak (Quercus sp.), Oyamel (Abies sp.) forest and biases in the model in MaxEnt software. The model high moor (CONANP, 2015). was evaluated with 10,000 bootstrap replicas and the This study began with the search for locations with “Raw output” was selected as the output file since this probability of occurrence of C. intermedius in the PONP is interpreted as the relative occurrence rate where each reported in other studies (Yáñez-Arenas et al., 2014); the cell has an environmentally important value for the information was used in the planning of the places where species, which were classified as low (<30), medium the search transects of the species would be developed (>30 and <60), and high (>60) probability of occurrence in the field. We searched the Global Biodiversity (González-Fernández et al., 2018). Additionally, the Information Facility database (GBIF, 2019) and found Jack-knife test was applied to determine the contribution 14 occurrences for all its geographic distribution area, of each variable to the model. We use a value greater of which two (14%) correspond to the state of Veracruz, than 0.9 of the Area Under the Curve (AUC) to evaluate four (29%) to the state of Puebla and eight (57%) to the effectiveness of the model (Nneji et al., 2019). the state of Oaxaca. In order to make a more realistic One way to validate potential distribution models is by modelling of the current biology of the species, we only corroborating the presence/absence of the species in the compiled the current records of C. intermedius (those geographic areas predicted by the model (Guevara et al., from the last 30 years). Therefore, we do not consider 2018). In this sense, once we obtained the C. intermedius historical records, since the objective of our model is potential distribution model, six people made five to forecast the expansion of species distribution under transects (5 km each) in four different locations within ongoing anthropogenic climate change (Guevara et the PONP. The transects started at 2,500 and ended at Altitudinal adaptation of Crotalus intermedius in a natural protected area, Mexico 885

Table 1. Annual averages for environmental variables in each of the records used in the Crotalus intermedius geographic distribution1 Table model. 1. Annual In eachaverages column, for environmental the minimum variables and maximum in each valuesof the records are given used in in bold. the Crotalus intermedius geographic 2 distribution model. In each column, the minimum and maximum values are given in bold. 3 Ocurrence Precipitation Temperature Evaporation Altitude (mm) (° C) (mm) (m a.s.l.) 1 370 13.9 357 2345 2 579 15.3 521 2087 3 1783 16 925 1766 4 1644 15.3 871 1800 5 1091 14.6 727 2345 6 965 15.7 720 2100 7 1582 12.9 746 2600 8 474 15.5 446 2273 9 1036 15 725 2300 10 693 11.6 528 2816

11 1304 14.4 752 2176 1 Table 1. Annual averages12 for environmental variables1381 in each of the12.9 records used in the714 Crotalus intermedius 2700 geographic 2 distribution model. In each column, the minimum and maximum values are given in bold. 3 13 780 18.9 690 1765 Ocurrence14 Precipitation799 Temperature12.8 Evaporation596 Altitude 2595 (mm) (° C) (mm) (m a.s.l.) Average 1034.36 14.63 665.57 2262 1 370 13.9 357 2345 Standard deviation 449.98 1.80 158.05 340.81 4 2 579 15.3 521 2087 5 3 1783 16 925 1766 6 4 1644 15.3 871 1800 7 4,5008 Tablem a.s.l., 2. Annual in which averages we5 lookedfor environmental for holes, variables trunks1091 inand each ofdistribution the14.6 field records map used727 indicated in model thatvalidation 2345 the PONPof Crotalus has 80% of 9 intermedius. In each column, the minimum and maximum values are given in bold. 6 965 15.7 720 2100 10sunny areas to determine the presence of C. intermedius its area characterised as low environmental importance specimens. The specimensField records7 captured used in werePrecipitation 1 identified582 andTemperature12.9 20% as mediumEvaporation746 or high 2600environmentalAltitude importance, based on the criteria proposedthe model8 validationby McCranie (1991)474(mm) and which15.5(° C) is interpreted446(mm) as the relative 2273(m a.s.l.) occurrence rate of the subsequently released. 91 10361903 species15 5.4 in the study7254 area80 (Fig. 2300 1). 4080 The distribution model 10 obtained2 presented6 93 AUC1947 = Based11.65.5 on the field5284 trips84 for 2816the 4000 validation of the model, 0.982 with the training data113 and AUC = 0.9721304 with1797 the three14.47 .3new locations752536 not known 2176 3640 for C. intermedius are test data, with a maximumAverage12 Receiver Operating13811882.3 Curve reported12.9 6.06 within the714500 PONP, which 2700 3906.6 were obtained in an (ROC) value of 0.956.Standard According13 deviation to the Jack-knife78077.1 test, area18.9 1.06with a low relative690 31.24 occurrence1765 234.37 rate, as predicted by the altitude variable contributed with 86.4% when it the model (Table 2). In the field, an adult individual of 11 14 799 12.8 596 2595 was used separately, while the remaining three variables ~300 mm in total length (TL) registered at 4,080 m a.s.l. Average 1034.36 14.63 665.57 2262 only contribute 13.6% in the model. The potential (18.9977°N, 97.3012°W; Datum WGS 84 – Fig. 2A) Standard deviation 449.98 1.80 158.05 340.81 4 5 6 Table7 2. Annual averages for environmental variables in each of the field records used in model validation of Crotalus intermedius. In8 eachTable column, 2. Annual the minimum averages andfor environmental maximum values variables are given in each in ofbold. the field records used in model validation of Crotalus 9 intermedius. In each column, the minimum and maximum values are given in bold. 10 1 Field records used in Precipitation Temperature Evaporation Altitude the model validation (mm) (° C) (mm) (m a.s.l.) 1 1903 5.4 480 4080 2 1947 5.5 484 4000 3 1797 7.3 536 3640 Average 1882.3 6.06 500 3906.6 Standard deviation 77.1 1.06 31.24 234.37 11

1

886 Ricardo Serna-Lagunes et al.

Figure 2. Specimens of Crotalus intermedius captured, identified and released in different localities in the Pico de Orizaba National Park (PONP), in Mexico.

was identified in the state of Puebla and two individuals According to Yáñez-Arenas et al. (2014) and based on in the state of Veracruz: an adult of ~330 mm TL the potential distribution model of C. intermedius, the (19.0018°N, 97.2453°W, 4,000 m a.s.l.; Datum WGS presence of the species was recorded in three locations 84 – Fig. 2B), and a juvenile of 180 mm TL (18.9850°N, not previously reported in the PONP (Fig. 2, Table 97.2479°W, 3,640 m a.s.l.; Datum WGS 84 – Fig. 2C). 2), which are classified in an asynotropy condition The vegetation where the C. intermedius individuals – confirmation of the species occurrence in a location were found was coniferous forest (Pinus hartwegii, not previously known within its range of potential Quercus laurina, and Abies religiosa) with the presence distribution (Zunino and Zullini, 2003). These new of a species commonly known as “zacaton” (Stipa reported locations represent an extension to the range of ichu), which forms a type of vegetation like that of high known altitudinal distribution reported for this species moorland. in other studies (2,000 m a.s.l. in Campbell and Lamar, Altitudinal adaptation of Crotalus intermedius in a natural protected area, Mexico 887

1989; 3,200 m a.s.l. in Campbell and Lamar, 2004; niche for its survival, although it is also possible that 2,109 m a.s.l. in Valencia-Hernández et al., 2007; 3,134 these individuals or populations have always been in the m a.s.l. in Fernández-Badillo et al., 2016), and even localities in which they were found, as it is more likely exceeds the altitudinal range reported to other viperid that they preferred to migrate to less disturbed areas, species: 2,560 m a.s.l. for C. aquilus Klauber, 1952; such as the core zone of the PONP, where the extraction 1,640 m a.s.l. for C. atrox Baird and Girard, 1853; of wood, hunting, agriculture, livestock and ecotourism 2,580 m a.s.l. for C. ravus Cope, 1865; 2,080 m a.s.l. are prohibited. for C. scutulatus Kennicott, 1861; and 1,320 m a.s.l. In Mexico, anthropogenic factors such as the use of for C. totonacus Gloyd and Kauffeld, 1940 (Valencia- rattlesnakes in rituals (Castellón-Huerta, 2001) and the Hernández et al., 2007). fact that the species is considered harmful to humans Since altitude is correlated with temperature, because of its venom (Ávila-Nájera et al., 2018), cause precipitation, and concentration of oxygen (Siegenthaler the death of many specimens of C. intermedius (Paredes- and Oeschger, 1980), there may be areas in the PONP García et al., 2011). Therefore, the lower limit for the with favourable thermal niche conditions for C. distribution of the species in the PONP may be around intermedius. The colonisation of thermal niches can be 2,600 m a.s.l. because it is where human settlements explained due to the displacement between areas of low are established and act as a barrier. A report recorded to adequate environmental suitability, thereby reducing the presence of C. intermedius at 2,571 m a.s.l. (Bryson the chronic harmful effects of temperature on normal and García-Vázquez, 2007), but the highest number of physiological functions such as mobility and embryo ophidian accidents associated with this species occurs development (Huang et al., 2007; Seok et al., 2017). in these localities (Almaráz-Vidal, 2016). This may The type of vegetation commonly known in Mexico represent a factor of local extinction of the species, but as “Paramo de Altura” (High Moor) in the PONP future studies should explore new areas at an altitude of is an area dominated by the presence of a species of less than 2,600 m a.s.l. to have a clearer diagnosis of the “zacatones” (Stipa ichu) distributed between 4,000 and true distribution of this species in the PONP. 5,000 m a.s.l. In this vegetation cover, we registered Given the importance of viperids per se and for three new sightings of C. intermedius. This type of being predators that are part of trophic plots and act vegetation cover may be a suitable habitat for C. as biological control (Campbell and Lamar, 2004), it intermedius, since the temperature, precipitation, and is imminent to generate conservation strategies for C. humidity remain constant throughout the year. The intermedius in the PONP and throughout its range of Paramo de Altura presents low richness and abundance distribution (Gutiérrez-Mayén, 2018). We propose of medium-sized mammals, but there is evidence that, that the strategy for the conservation of this species in this vegetation, the abundance of rodents is greater should focus on the management of the habitat. than in the other types of vegetation that converge in the Therefore, it is necessary to limit access to grazing by PONP (Serna-Lagunes et al., 2019). So, it is possible livestock in the highland vegetation. This will prevent that low competition and wide availability of resources cows from trampling the shelters that the species favour the establishment of C. intermedius in this type occupies. Another important aspect is to generate an of vegetation. environmental education program to raise awareness of The Paramo de Altura in the PONP is the type of the human communities that inhabit the PONP to make vegetation with the highest risk of surface loss, due to a non-extractive use of the environment that helps the fires and the change of land use for the development conservation of the species and its habitat. of productive activities (agriculture and livestock), which have caused the fragmentation, reduction or Acknowledgements. We are grateful to the project transformation of the environment, and even the loss “Caracterización de recursos zoogenéticos de la región de Las of native vegetation (Ávila-Bello, 1996). These factors Altas Montañas, Veracruz: implicaciones de la modelación ecológica y la filogeografía” (SEP-511-6/18-9245/PTC-896) for occasioned the loss of biological diversity and, probably, partial financing for field activities. Comisión Nacional de Áreas led to reduction of the species distribution area or Naturales Protegidas (CONANP) of the PONP for the suggestions modification of the distribution areas due to microclimate issued during the fieldwork. change in the PONP (CONANP, 2014, 2015). This may be another reason why C. intermedius has moved to higher altitudes where it finds a favourable ecological 888 Ricardo Serna-Lagunes et al.

References México. Proyecto: DS009, Extraído del proyecto DS009: Áreas potenciales de distribución y GAP análisis de la herpetofauna de Aldape-López, C.T., Santos-Moreno, A. (2016): Efecto del manejo México. El proyecto fue financiado por la Comisión Nacional forestal en la herpetofauna de un bosque templado del occidente para el Conocimiento y Uso de la Biodiversidad (CONABIO). de Oaxaca, México. Revista de Biología Tropical 64: 931–943. México. Almaráz-Vidal, D. (2016): Las serpientes venenosas de importancia Fernández-Badillo, L., Olvera-Olvera, C., Torres-Ángeles, F. médica de la región de Las Grandes Montañas de Veracruz, (2016): Distribution Note. Mesoamerican Herpetology 3 (2): México: aspectos ecológicos y accidentes ofídicos. Revista 256–256. Mundo Investigación 2 (1): 173–180. Fernández-Eguiarte, A., Romero-Centeno, R., Zavala-Hidalgo, Angilletta, M.J. (2001): Thermal and physiological constraints J. (2012): Libro electrónico: Atlas Climático de México y on energy assimilation in a widespread lizard (Sceloporus Áreas Adyacentes. Volumen 1. Unidad de Informática para las undulatus). Ecology 82: 3044–3056. Ciencias Atmosféricas y Ambientales (UNIATMOS), Centro de Ávila-Bello, C.H. (1996): Notes on an agricultura system at the Ciencias de la Atmósfera. Universidad Nacional Autónoma de Pico de Orizaba, Veracruz, Mexico. Botanical Sciences 59: México. Servicio Meteorológico Nacional, Comisión Nacional 59–66. del Agua. 204 pp. Ávila-Nájera, D.M., Mendoza, G.D., Villarreal, O., Serna-Lagunes, García, E. (1988): Modificaciones al sistema de clasificación R. (2018): Uso y valor cultural de la herpetofauna en México: climática de Köppen. Ciudad de México, México, Universidad una revisión de las últimas dos décadas (1997-2017). Acta Nacional Autónoma de México. Zoológica Mexicana (nueva serie) 34: 1–15. GBIF (2019): Crotalus intermedius. In: Gutiérrez-Mayén, M.G. Boyle, M., Schwanz, L., Hone, J., Georges, A. (2016): Dispersal Herpetofauna de la reserva de la biósfera Valle de Tehuacán- and climate warming determine range shift in model reptile Cuicatlán (etapa final). Comisión Nacional para el Conocimiento populations. Ecological Modelling 328: 34–43. y Uso de la Biodiversidad. Occurrence dataset availabe at: Bryson, R.W., Murphy, R.W., Graham, M.R., Lathrop, A., Lazcano, https://doi.org/10.15468/xaavwk Accessed via GBIF.org on 04 D. (2011): Ephemeral Pleistocene woodlands connect the dots May 2019. for highland rattlesnakes of the Crotalus intermedius group. González-Fernández, A., Manjarrez, J., García-Vázquez, U., Journal of Biogeography 38 (12): 2299–2310. D’Addario, M., Sunny, A. (2018): Present and future ecological Bryson, R.W., García-Vázquez, U.O. (2007): Geographic niche modeling of garter snake species from the Trans-Mexican distribution. Crotalus intermedius gloydi. Herpetological Volcanic Belt. PeerJ 6: e4618. Review 38 (3): 354–355. Gutiérrez-Mayén, M.G. (2018): Inventario herpetofaunístico del Caballero, M., Lozano-García, S., Vázquez-Selem, L., Ortega, B. valle semiárido de Tehuacán-Cuicatlán (continuación). Comisión (2010): Evidencias de cambio climático y ambiental en registros Nacional para el Conocimiento y Uso de la Biodiversidad. glaciales y en cuencas lacustres del centro de México durante Occurrence dataset available at: https://doi.org/10.15468/ el último máximo glacial. Boletín de la Sociedad Geológica mb678i Accessed via GBIF.org on 04 May 2019. iNaturalist.org Mexicana 62 (3): 359–377. (2019). iNaturalist Research-grade Observations. Occurrence Campbell, J.A., Lamar, W.W. (1989): The venomous reptiles of dataset https://doi.org/10.15468/ab3s5x accessed via GBIF.org Latin America. New York, USA, Cornell University. on 2019-05-04. Campbell, J.A., Lamar, W.W. (2004): The venomous reptiles of Guevara, L., Gerstner, B.E., Kass, J.M., Anderson, R.P. (2018): the Western Hemisphere. Vol. II. London, England, Comstock Toward ecologically realistic predictions of species distributions: Publishing Associates. Cornell University. A cross-time example from tropical montane cloud forests. Canseco-Márquez, L., Campbell, J.A., Ponce-Campos, P., Global Change Biology 24 (4): 1511–1522. Muñoz-Alonso, A., García-Aguayo, A. (2007): Crotalus Hernández-Jandete, F., Fernández-Badillo, H., Ibarra-Bautista, A., intermedius. The IUCN Red List of Threatened Species 2007: Olvera-Olvera, R. (2017): Crotalus intermedius. Distribution e.T64319A12766370. Available at: http://dx.doi.org/10.2305/ note. Mesoamerican Herpetology 4 (3): 678–679. IUCN.UK.2007.RLTS.T64319A12766370.en. Accessed on 20 Huang, S.M., Huang, S.P., Chen, Y.H., Tu, M.C. (2007): Thermal November 2019. tolerance and altitudinal distribution of three Trimeresurus Castellón-Huerta, B. (2001): Cúmulo de símbolos. La serpiente snakes (Viperidae: Crotalinae) in Taiwan. Zoological Studies 46 emplumada. Arqueología Mexicana 53: 28–35. (5): 592–599. CONANP (2014): Anteproyecto del Programa de Manejo Parque López-Colladom, J. (2020): Control de calidad de puntos de Nacional Pico de Orizaba. Distrito Federal, México, Comisión muestreo georreferenciados. Accessed via https://sites.google. Nacional de Áreas Naturales Protegidas. com/site/diaphorina/qualitycontrolgi on 03 June 2020. CONANP (2015): Programa de Manejo Parque Nacional El Pico Manzanilla-Quiñones, U., Aguirre-Calderón, Ó.A., Jiménez de Orizaba. Distrito Federal, México, Comisión Nacional de Pérez, J., Treviño-Garza, E.J., Yamallel, Y., Israel, J. (2018): Áreas Naturales Protegidas. Escenarios de cambio climático (CMIP-5) para tres áreas Correa-Cano, M.L., Ochoa-Ochoa, L., Flores-Villela, O., García- naturales protegidas en el Eje Neovolcánico Transversal. Revista Vázquez, U., Canseco-Márquez, L. (2009): Crotalus intermedius Mexicana de Ciencias Forestales 9 (50): 514–537. (Víbora cascabel enana). Área de distribución potencial, McCranie, J.R. (1991): Crotalus intermedius Troschel Mexican escala: 1:1000000. Museo de Zoología Alfonso L. Herrera, Small-headed Rattlesnake. Catalogue of American Amphibians Facultad de Ciencias, Universidad Nacional Autónoma de and Reptiles 1991: 519.1–5194. Altitudinal adaptation of Crotalus intermedius in a natural protected area, Mexico 889

Nneji, L.M., Adeola, A.C., Yan, F., Okeyoyin, A.O., Oladipo, O.C., Siegenthaler, U., Oeschger, H. (1980): Correlation of 18O in Saidu, Y., et al. (2019): Genetic variation and cryptic lineage precipitation with temperature and altitude. Nature 285 (5763): diversity of the Nigerian red headed rock agama (Agama 314. agama) associate with eco-geographic zones. Current Zoology Urbina-Cardona, J.N., Flores-Villela, O. (2010): Ecological-niche 022019: 1–12. modeling and prioritization of conservation-area networks for Paredes-García, D.M., Ramírez-Bautista, A., Martínez-Morales, Mexican herpetofauna. Conservation Biology 24 (4): 1031– M.A. (2011): Distribución y representatividad de las especies 1041. del género Crotalus en las áreas naturales Protegidas de México. Urbina-Cardona, J.N. (2016): Gradientes andinos en la diversidad Revista Mexicana de Biodiversidad 82: 689–700. y patrones de endemismo en anfibios y reptiles de Colombia: Phillips, S.J., Anderson, R.P., Schapire, R.E. (2006): Maximum posibles respuestas al cambio climático. Revista Facultad de entropy modeling of species geographic distributions. Ecological Ciencias Básicas 7 (1): 74–91. Modelling 190 (3): 231–259. Valencia-Hernández, A.A., Goyenechea, I., Castillo-Cerón, J. Phillips, S.J., Dudík, M. (2008): Modeling of species distributions (2007). Notes on scutellation, length, and distribution on with Maxent: new extensions and a comprehensive evaluation. rattlesnakes in the state of Hidalgo, Mexico. Acta Zoológica Ecography 31 (2): 161–175. Mexicana (nueva serie) 23 (3): 29–33. Seok, M.D., Ki-Baek, N., Jeong-Chil, Y. (2017): Distribution and Yáñez-Arenas, C., Peterson, A.T., Mokondoko, P., Rojas-Soto, movement tendencies of Short-Tailed Viper Snakes (Gloydius O., Martínez-Meyer, E. (2014): The use of ecological niche saxatilis) by altitude. Asian Herpetological Research 8 (1): modeling to infer potential risk areas of snakebite in the Mexican 39–47. state of Veracruz. PLoS ONE 9 (6): e100957. Secretaría De Medio Ambiente y Recursos Natura les Zunino, M., Zullini, A. (2003): Biogeografía: la dimensión espacial (SEMARNAT) (2010): Norma Oficial Mexicana NOM-059- de la evolución. Distrito Federal, México. Fondo de Cultura SEMARNAT-2010. Protección Ambiental-Especies nativas Económica. de México de flora y fauna silvestres-Categorías de riesgo y especificaciones para su inclusión, exclusión o cambio. Lista de especies en riesgo. Ciudad de México, México. Serna-Lagunes, R., Álvarez-Oseguera, L.R., Ávila-Nájera, D.M., Leyva-Ovalle, O.R., Andrés-Meza, P., Tigar, B. (2019): Temporal overlap in the activity of Lynx rufus and Canis latrans and their potential prey in the Pico de Orizaba National Park, Mexico. Animal Biodiversity and Conservation 42 (1): 153–161.

Accepted by Pedro Pinna