Research Article |
Corresponding author: Armando Sunny ( sunny.biologia@gmail.com ) Academic editor: Günter Gollmann
© 2019 Armando Sunny, Fabiola J. Gandarilla-Aizpuro, Octavio Monroy-Vilchis, Martha M. Zarco-Gonzalez.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Sunny A, Gandarilla-Aizpuro FJ, Monroy-Vilchis O, Zarco-Gonzalez MM (2019) Potential distribution and habitat connectivity of Crotalus triseriatus in Central Mexico. Herpetozoa 32: 139-148. https://doi.org/10.3897/herpetozoa.32.e36361
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The dusky rattlesnake, Crotalus triseriatus, used to be very abundant in many parts of the highlands of central Mexico, but with the increasing human population and associated activities, the rattlesnake habitats and populations have suffered drastic reductions and fragmentation. At the moment, the most important habitat features, associated with the presence of C. triseriatus, the current potential distribution and the landscape connectivity amongst the populations of the State of Mexico and Mexico City, are unknown. Therefore, we used the maximum entropy modelling software (MAXENT) to analyse the current potential distribution and most important habitat features, associated with the presence of the species. The variables with the highest contribution to the model were: proportion of Abies forest, minimum temperature of coldest month, maximum temperature of the warmest month, proportion of Pinus forest and annual precipitation. Furthermore, we found connectivity corridors only within mountain chains. Our results highlight the necessity for conserving the patches of Abies forest and preserving the populations of C. triseriatus and the connectivity of the landscape.
Früher war Crotalus triseriatus in vielen Teilen des Hochlandes von Zentralmexiko häufing, aber mit der wachsenden Bevölkerung und den damit verbundenen Aktivitäten haben die Lebensräume und die Populationen der Klapperschlangen drastische Rückgänge und Fragmentierungen erfahren. Derzeit wissen wir nicht, welche Habitatmerkmale am wichtigsten für das Auftreten von C. triseriatus, seine aktuelle potentielle Verbreitung und die landschaftlichen Konnektivität zwischen den Populationen des Staates Mexiko und Mexiko- Stadt sind. Aus diesem Grund haben wir die Maximum-Entropy-Modellierungssoftware (MAXENT) verwendet, um die aktuelle potenzielle Verbreitung und die wichtigsten Habitatmerkmale zu ermitteln, die mit dem Vorkommen der Art zusammenhängen. Die Variablen mit dem höchsten Beitrag zum Modell waren: Anteil des Abies-Waldes, minimale Temperatur des kältesten Monats, maximale Temperatur des wärmeren Monats, Anteil des Pinus-Waldes und jährlicher Niederschlag, und wir fanden Verbindungskorridore nur innerhalb von Gebirgsketten. Als Fazit ist es notwendig, die Bestände des Abies-Waldes und die Populationen von C. triseriatus und die Konnektivität der Landschaft zu erhalten.
circuit theory, ecological niche modelling, habitat fragmentation, habitat suitability, protected natural areas
The conservation and management of species require basic information on their geographic distribution, ecology and abundance of populations. In recent years, ecological niche modelling (ENM) has been widely used to assess geographic distribution of species at different scales for conservation purposes, with reliable results (
Rattlesnakes are abundant in many parts of Mexico and have a wide distribution spread around the country (
Most populations of C. triseriatus, as well as other species of this group, have declined due to urban development, hunting and habitat loss (
In order to propose conservation strategies for C. triseriatus, it is essential to address the environmental requirements and precise distribution of C. triseriatus, as well as the degree of fragmentation of their habitats. Consequently, our research questions are: 1) what are the environmental requirements of C. triseriatus; 2) which are the most important habitat features associated with the presence of the species; 3) what is the current potential distribution of C. triseriatus in central Mexico; and finally, 4) what is the degree of landscape connectivity amongst populations of C. triseriatus in the State of Mexico and Mexico City? These results will provide valuable information for management decisions orientated towards helping to preserve this endemic species.
Field work was conducted at 24 sites in the State of Mexico and Mexico City (Fig.
For ENM, a database of records on the geographical distribution of the species was compiled. After an autocorrelation test using the software NICHE TOOLBOX (
Habitat variables in percentage of habitat in a 1×1 km cell, considered for the ENM and landscape connectivity resistance map.
Variable | Units | Source | Author(s) | Year |
---|---|---|---|---|
Proportion of agriculture | % | National forest inventory | INEGI | 2013 |
Proportion of cloud forest | % | National forest inventory | INEGI | 2013 |
Proportion of Abies forest | % | National forest inventory | INEGI | 2013 |
Proportion of Quercus forest | % | National forest inventory | INEGI | 2013 |
Proportion of Quercus-Pinus forest | % | National forest inventory | INEGI | 2013 |
Proportion of Pinus forest | % | National forest inventory | INEGI | 2013 |
Proportion of Pinus-Quercus forest | % | National forest inventory | INEGI | 2013 |
Proportion of grassland | % | National forest inventory | INEGI | 2013 |
Distance to water sources | km | National forest inventory | INEGI | 2013 |
Distance to settlements | km | National forest inventory | INEGI | 2013 |
Altitude | MASL | Digital elevation model | USGS | 2007 |
Annual precipitation | mm | WorldClim | Hijmans et al. | 2005 |
Maximum temperature of the warmest month | °C | WorldClim | Hijmans et al. | 2005 |
Minimum temperature of the coldest month | °C | WorldClim | Hijmans et al. | 2005 |
We applied the Maximum Entropy algorithm using MAXENT software (
For the landscape connectivity, we modelled patterns of population connectivity using circuit theory, where population connectivity is analogous to an electrical current (
For the ENM, we obtained 24 records (Fig.
The MAXENT model performed better than expected by random, where the AUC showed high average values across iterations (AUC = 0.990 P = 0.001). Additionally, the partial-ROC bootstrap test showed significant ratio values of empirical AUC over null expectations (ratio = 1.437; P = 0.001). The model (Fig.
Potential distribution of C. triseriatus identified using ENM in the State of Mexico and Mexico City. 1. Iztaccíhuatl-Popocatépetl-Zoquiapan, 2. Sierra de las Cruces, 3. The Corredor Biológico Chichinautzin, 4. The Nevado de Toluca Volcano and 5. Reserva de la Biósfera Santuario Mariposa Monarca.
The variables with the highest contribution to the model were: Abies forest, minimum temperature of the coldest month, maximum temperature of the warmest month, Pinus forest and annual precipitation; together, these variables explained 83.4% of the variation in species distribution (Table
Average contribution percent of variables according MAXENT, the Interval of occurrence that explain the distribution of C. triseriatus and the standard deviations of the contribution percent of variables according MAXENT.
Variable | Contribution to the model | Interval of C. triseriatus occurrence | Standard deviation |
---|---|---|---|
Abies forest | 25.1% | 10–90% | 0.069 |
Minimum temperature of coldest month | 19.6% | -1–12 °C | 0.351 |
Maximum temperature of the warmest month | 17.1% | 5–27 °C | 0.104 |
Pinus forest | 13.3% | 10–100 % | 0.041 |
Annual precipitation | 8.3% | 500–1600 mm | 0.336 |
Pinus-Quercus forest | 6.7% | 10–100 % | 0.051 |
Altitude | 4.1% | 2000–4600MASL | 0.262 |
Distance to settlements | 3.4% | 0–32.5 km | 0.046 |
Quercus forest | 1.6% | 0–30% | 0.263 |
Distance to water sources | 0.3% | 0–28 km | 0.106 |
Grassland | 0.2% | 0–90% | 0.102 |
Cloud forest | 0.2% | 0–65% | 0.274 |
Agriculture | 0% | 0–95% | 0.116 |
Quercus-Pinus forest | 0% | 0–100% | 0.268 |
ENM resistance surfaces showed connectivity corridors principally within mountain chains (Fig.
Connectivity maps among 24 studied sites for C. triseriatus. The resistance map was estimated using CIRCUITSCAPE and based on habitat suitability from ENM reconstructions. Red and green indicates areas with higher current density; areas where connectivity is most tenuous are shown in lighter oranges. 1. Iztaccíhuatl-Popocatépetl-Zoquiapan, 2. Sierra de las Cruces, 3. The Corredor Biológico Chichinautzin, 4. The Nevado de Toluca Volcano and 5. Reserva de la Biósfera Santuario Mariposa Monarca.
According to ENM and the resistance surface, C. triseriatus populations have a highly fragmented distribution with low values of connectivity, mostly restricted within the Abies-Pinus forest of the mountain chains of the State of Mexico and Mexico City. The Abies-Pinus forests were highly important variables according to ENM, being Abies the first and Pinus the fourth most important variables. The Trans-Mexican Volcanic Belt has the highest amount of Abies forest (91.143%) and a great percentage of Pinus forest (29.657%) of the country, however these types of forests are scarce in the Trans-Mexican Volcanic Belt, where only 1.1% of Abies forest and 5.4% of Pinus forest cover the biogeographic zone. Therefore, it is essential to establish conservation plans to preserve this habitat, since good quality habitat maintains high levels of genetic diversity in the populations of C. triseriatus (
Likewise, Abies forest is highly correlated with the C. triseriatus distribution, likely because these two species evolved together when this biogeographic province was formed in the Neogene; in fact, the uplifting of the Trans-Mexican Volcanic Belt is considered one of the most important forces driving the evolutionary history of several taxa (
These species have adapted to high cold mountain environmental conditions (
The ENM shows that C. triseriatus populations have a highly fragmented distribution for several reasons: one possible explanation is that the habitat, which this species prefers, is high mountain areas within the Abies-Pinus forests that are historically isolated (
Although there are stable populations in the agriculture fields, large rattlesnakes have insufficient refuges and a variety of vegetation cover to allow the exploitation of thermal gradients (
It is also important that populations are not isolated in small patches of habitat (
In order to preserve the populations of C. triseriatus that live in the matrix of agriculture and urbanisation, it is necessary to leave rocks, shrubs and pastures around agriculture fields and leave native trees in order to create shelters with different microhabitats that generate thermal gradients; it is important to avoid the burning of pastures, since, apart from killing the biodiversity that lives in these pastures (C. triseriatus: dusky rattlesnake, Barisia imbricate: Imbricate Alligator Lizard, Sceloporus torquatus: Torquate Lizard Mountain, Dryophytes eximius: Treefrog, amongst others), around 5–10% of overall air pollution mortalities are due to the burning of biomass (
The populations found in the mountain ranges have moderate to low levels of connectivity, mainly in the mountains of Iztaccíhuatl-Popocatépetl-Zoquiapan volcanoes and the Biosphere Reserve Monarch Butterfly Sanctuary is totally disconnected from any other population of C. triseriatus. It can also be observed that areas of high suitability found in Sierra de las Cruces and the Corredor Biológico Chichinautzin are outside protected areas.
It would be important to carry out landscape genetic studies to find out how fragmentation and isolation of the populations could be affecting the populations of C. triseriatus. The only population genetics study was carried out in the Nevado de Toluca Volcano and the results showed that the populations present moderate to high levels of genetic diversity (
In conclusion, the preservation of C. triseratus will require the increase and maintenance of the connectivity amongst areas of habitation, as well as the protection of other species that harness these corridors. To maintain and improve positive results on conservation efforts, constant research is required on ecological traits and population parameters (e.g. connectivity, diversity) of this species, as well as predictive modelling to anticipate population dynamics under future climate change scenarios. Finally, it is important to conduct dissemination of information within the human populations that share the habitat with this species. Environmental education talks are expected to prevent the further killing of snakes out of fear or for medicinal or ritual purposes.
We are grateful to the editor Günter Gollmann and three anonymous reviewers for their comments that helped to improve the manuscript. We thank Andrea González-Fernández for the analysis advice and for help with field work. We thank Xareni P. Pacheco for valuable English editing. The manipulation of rattlesnakes was conducted with the approval of the ethics committee of the Autonomous University of the State of Mexico (DCARM-2014; 9855714) and the field permit: SGPA / DGVS / 011587/17 SEMARNAT.