The Impact of Global Warming on the Range Distribution of Different Climatic Groups of Aspidoscelis costata costata

Author(s): Martha Anah Gizado-Rodrguez , Claudia Ballesteros-Barrera , Gustavo Casas-Andreu , Victor Luis Barradas-Miranda , Oswaldo Tllez-Valds and Isaas Hazarmabeth Salgado-Ugarte Source: Zoological Science, 29(12):834-843. 2012. Published By: Zoological Society of Japan DOI: http://dx.doi.org/10.2108/zsj.29.834 URL: http://www.bioone.org/doi/full/10.2108/zsj.29.834

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ZOOLOGICAL SCIENCE 29: 834843 (2012)

2012 Zoological Society of Japan

The Impact of Global Warming on the Range Distribution of Different Climatic Groups of Aspidoscelis costata costata
Martha Anah Gizado-Rodrguez1*, Claudia Ballesteros-Barrera2, Gustavo Casas-Andreu1, Vctor Luis Barradas-Miranda3, Oswaldo Tllez-Valds4, and Isaas Hazarmabeth Salgado-Ugarte2,5
Departamento de Zoologa, Instituto de Biologa, Universidad Nacional Autnoma de Mxico, Circuito Exterior s/n, AP 70-153, Mxico D.F. 04510 2 Departamento de Biologa, Universidad Autnoma Metropolitana Iztapalapa, A.P 55-35, Avenida San Rafael Atlixco #186 Colonia Vicentina, Delegacin Iztapalapa, Mxico D.F. 09340 3 Departamento de Ecologa Funcional, Instituto de Ecologa, Universidad Nacional Autnoma de Mxico, Circuito Exterior s/n, AP 70-153, Mxico D.F. 04510 4 Laboratorio de Recursos Naturales Unidad de Biologa, Tecnologa y Prototipos, Facultad de Estudios Superiores Iztacala, Universidad Nacional Autnoma de Mxico, Avenida de los Barrios 1, Los Reyes Iztacala, Tlalnepantla, Estado de Mxico, 54090 5 Laboratorio de Biometra y Biologa Pesquera, Facultad de Estudios Superiores Zaragoza Campus II, Universidad Nacional Autnoma de Mxico, Batalla 5 de mayo s/n esq. Fuerte de Loreto Col. Ejrcito de Oriente, Mxico D.F. 09230
1

The ectothermic nature of reptiles makes them especially sensitive to global warming. Although climate change and its implications are a frequent topic of detailed studies, most of these studies are carried out without making a distinction between populations. Here we present the first study of an Aspidoscelis species that evaluates the effects of global warming on its distribution using ecological niche modeling. The aims of our study were (1) to understand whether predicted warmer climatic conditions affect the geographic potential distribution of different climatic groups of Aspidoscelis costata costata and (2) to identify potential altitudinal changes of these groups under global warming. We used the maximum entropy species distribution model (MaxEnt) to project the potential distributions expected for the years 2020, 2050, and 2080 under a single simulated climatic scenario. Our analysis suggests that some climatic groups of Aspidoscelis costata costata will exhibit reductions and in others expansions in their distribution, with potential upward shifts toward higher elevation in response to climate warming. Different climatic groups were revealed in our analysis that subsequently showed heterogeneous responses to climatic change illustrating the complex nature of species geographic responses to environmental change and the importance of modeling climatic or geographic groups and/or populations instead of the entire species range treated as a homogeneous entity. Key words: Aspidoscelis costata costata, global warming, climatic groups, MaxEnt, altitudinal distribution INTRODUCTION The geographic distribution of animals and plants is determined by ecological and historical factors (Begon et al., 1996; Hawkings and Porter, 2003). A growing body of data indicates that reptilian populations have seen elevated declines worldwide mainly due to habitat loss and degradation, introduced invasive species, environmental pollution, disease and parasitism, unsustainable use, and global climate change (Gibbons et al., 2000; Sinervo et al., 2010). Mexico is considered a megadiverse country, particu* Corresponding author. Tel. : +52(55)56-22-91-47, Ext. 47820; Fax : +52(55)55-50-01-64; E-mail: anahigr@ibunam2.ibiologia.unam.mx doi:10.2108/zsj.29.834

larly in terms of reptilian diversity as it is home to 804 (9.76%) of the 8,238 described species worldwide (FloresVillela and Canseco-Mrquez, 2004). However, more than 50% of these reptilian species are considered to be at some level of risk by Mexican Official Norm (NOM-059-SEMARNAT2010 see www.ine.gob.mx). Among the factors of greater threat to Mexican reptilian biodiversity is global warming, although even today this issue is relatively unexplored (Sinervo et al., 2010). The Earth has experienced climatic perturbations promoting an environmental temperature increase of 0.74C over the last 100 years (IPCC, 2007). This warming has induced biological and ecological responses in animals and plants. Consistent responses are apparent in phenology (McCarty, 2001; Parmesan, 2006), life history traits (Chammaill-Jammes et al., 2006; Lepetz et al., 2009), and

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geographic distributions (Blaustein et al., 2001; Shoo and Williams, 2004) at range margins both in latitude (Hickling et al., 2006; Parmesan, 2006) and altitude (Gian-Reto et al., 2005; Raxworthy et al., 2008), and even in depth for marine fishes (Perry et al., 2005). However, testing the hypothesis that climate warming is causing species declines is challenging given that many interacting processes operate at different spatial scales and the responses are clearly species and population-dependent (Arajo et al., 2006). Most studies addressing this issue focus only on a portion of the species range and fewer still analyze the response of more than one population (Chamaill-Jammes et al., 2006; Foden et al., 2007). In Mexico, climate change scenarios show there to be a tendency to dryness with a temperature increase of 2C and a decrease of 10% in precipitation due to global warming (Villers-Ruiz and Trejo-Vzquez, 2004). The effects of these climatic changes on the genus Aspidoscelis remain unexplored even though it is among the most diverse lizard groups inhabiting Mexico. Aspidoscelis costata belongs to the sexlineata group, which is the most diverse clade within the genus Aspidoscelis. This species is comprised of eight subspecies: A. c. barrancorum, A. c. costata, A. c. zweifeli, A. c. huico, A. c. occidentalis, A. c. griseocephalus, A. c. mazatlanensis and A. c. nigrigularis (Reeder et al., 2002). Aspidoscelis costata costata (Cope, 1877), the focal species of our study, is an endemic lizard of Mexico with a wide altitudinal range of 5282468 m above sea level (Duellman and Zweifel, 1962; Maslin and Walker, 1965; RodrguezRomero et al., 2003; Walker, 2003). As a result it is exposed to broad array of selection pressures, making it a suitable model for testing a population-dependent response due to global warming. In this paper, we aimed to explain the potential impacts of climate change by modeling potential distributions and the altitudinal variation of different climatic groups of A. c. costata across its full distributional range. Specifically, we 1) compared current and future potential distributions to assess whether suitable climate space is projected to increase or decrease with climate change, and 2) evaluated the potential altitudinal variation under a simulated climatic scenario. MATERIALS AND METHODS
Data sources Species records consist of individual point-locality information that is presence-only data obtained from fieldwork and 24 national and international museum collections (see Acknowledgments) and some related references (Maslin and Walker, 1965; RodrguezRomero et al., 2003; Walker, 2003). The data set consisted of 4565 records, which represent 158 different distributional points for A. c. costata. The sampling period of the locality records was from 1937 to 2007. When necessary, BioGeoMancer (http://classic.biogeomancer. org) and the Global Gazetteer V2.2 were used for georeferencing. Selection of climatic groups We choose climatic groups (CG) using a Bioclim extension in the GIS (Geographic Information System) Arc View 3.2 (ESRI) based on the principle that geographic limits can be predicted for a species according to its bioclimatic preferences (Nix, 1986). We generated a bioclimatic profile that was classified by the hierarchical association of the PATN program, using the Gower Index and the UPGMA association option. Finally, we obtained a cluster of localities by contrasting climates that allowed us to identify different CG.

We then performed a discriminant function analysis and obtained Mahalanobis distances between groups to validate the non-random occurrence of the constituted groups and to test for similarity between them using the Statistica 9 Software (StatSoft, 2010). With the previous analysis, we verified whether the CG were climatologically different, and modeled their projected distributions under our chosen climatic scenario. Climate variable selection Distribution models were generated using different environmental surfaces: 1) topographic data including aspect (i.e. the direction to which a mountain slope faces), slope (i.e. the amount of inclination of a surface to the horizontal plane), and topographic index (i.e. the soil capacity for water retention) (U. S. Geological Survey; http://edcdaac.usgs.gov/gtopo30/hydro/); and 2) environmental data obtained from Worldclim (Hijmans et al., 2005; http://www.worldclim. org) at a spatial resolution of ~1 km2. These climate data are derived from meteorological monthly temperature and rainfall values from 1950 to 2000 and represent biologically meaningful variables for characterizing species distributions (Nix, 1986). The Worldclim data layers included 11 temperature and eight precipitation metrics representing spatial variation in annual means and extremes. We performed principal component analysis (PCA) using the Statistica 9 Software (StatSoft, 2010) to investigate how different environmental variables co-varied in order to reduce variable redundancy in the model (Beaumont et al., 2005). The Aspidoscelis costata costata locality records constitute all that is known about its distribution. However, this species is likely to have been distributed in other areas in which it was not detected in the past, or is likely to occur in other areas in which it has not yet been detected at present. Therefore, we thought that the impact of global warming is in progress and the sampling period of locality records that we used to forecast current potential distribution is according to the period of time that was used to model construction as current climate. Modeling method There is a suite of methods to model the ecological niche of a species (Elith et al., 2006). Essentially, it is a technique used to estimate actual or potential areas of distribution, or sets of favorable habitats for a given species, on the basis of its observed presence and (sometimes) absence at different localities, jointly with digital maps (GIS raster layers) of environmental variables (Sobern and Nakamura, 2009). The niche modeling approach outlines the potential ecological distributions onto Hutchinsons fundamental niche concept as opposed to the realized niche space (Sobern and Peterson, 2005), which takes into account the limiting effects of biological interactions (Hutchinson, 1957). We used the maximum entropy species distribution model (Philips et al., 2004, 2006) as implemented in the software MaxEnt version 3.3.1 (freely available at http://www.cs.princeton.edu/ wschapire/maxent/). This niche modeling has been used in several studies to predict species distributions (Zonneveld et al., 2009; Wang et al., 2010; Weinsheimer et al., 2010). MaxEnt calculates the distribution of maximum entropy for a species within a given area based on observed climate values at locations where the species has been reported. The output model is a cumulative probability of occurrence expressed as a percentage (Phillips et al., 2006). There is no formal procedure to assign a certain percentage to training and testing data set, because these percentages are related to the number of species records. According to Stockwell and Peterson (2002), improvement of model performance takes place at 20 data points. Therefore we assigned 50% of our data for training and 50% for testing to generate potential distribution maps for those CG with more than 50 records of point localities. In the case of CG with less than 50 points, we assigned 100% of point localities to the training data set. The files produced were mapped as raster grids of 1 km2 of spatial resolution to produce ARCINFO/

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ASCII/GRID files, which were edited with the GIS ArcView 3.2 (ESRI). In order to create a binary map of presence/absence of the species we used the minimum cumulative value of training sample points as a threshold value (Phillips et al., 2006). Using the cut-off value, models were classified into binary (1 or 0) or presenceabsence model. We used the receiver operating characteristic curve (ROC) to examine model performance calculating the area under the receiver operating curve (AUC) which measure the ability of a model to discriminate between sites where a species is present versus those where it is absent. AUC ranges from 0 to 1 where a score of 1 indicates perfect discrimination generally, AUC values greater than 0.7 are considered to be potentially significant, while scores of 0.5 imply discrimination that is no better than random (Elith et al., 2006). Future potential distribution We used the same topographic and climatic data that were chosen for modeling current potential distribution to project future potential distributions. Future climate data was derived from GCM (General Circulation Models) projections for the years 2020, 2050 and 2080 from the CGCM2SRES model under the A2 emission scenario which is based on projections produced by the Canadian Climate Centre (http://www.ipcc-data.org/sres/gcm_data.html) at a spatial resolution of 0.01 0.01 (~1 km2) (Flato et al., 2000). The A2 scenario (liberal model) is described as a very heterogeneous world. It is based on strengthening regional cultural identities, high population growth, and less concern for rapid economic development. This scenario predicts an environmental temperature increase of 3.0 to 5.2 C for 2100 y (IPCC, 2007). We chose the A2 emission scenario because it is one of the most extreme climate scenarios to predict a high increase in environmental temperature. For Aspidoscelis, it could be challenging to live under these climate conditions. This genus has one of the highest body temperatures among reptiles (i.e. 40C, Vitt and Pianka, 2004); therefore they already live close to their optimal body temperature. Moreover this scenario has been used in other studies investigating the effect of climate change on lizard distributions (Ballesteros-Barrera et al., 2007). Altitudinal variation To evaluate the potential altitudinal variation of each CG, we converted each grid of every current and future potential distribution map into a point. After that, each map was overlaid onto an elevation digital model with a resolution of ~1 km2 to obtain current and future altitudinal grid values. We next used a violin plot as an exploratory tool of the altitudinal data distribution, to reveal the structure found within the data (Hintze and Nelson, 1998). A violin plot is a combination of a box plot and a kernel density plot. Specifically, it starts with a box plot and then it adds a rotated kernel density plot to each side of the box plot. Violin plots include the median of the data and a box indicating the interquartile range, as in standard box plots. Individually, box plots provide succinct summaries of data. By themselves, density traces reveal important information about the distribution of data. The synergistic combination of the box plot and the density trace allows much of the information from each to be displayed in one plot. This single plot structure makes comparisons of distributional factors of several variables much easier (Hintze and Nelson, 1998). Next, we used a kernel density estimator (KDE) for exploring and analyzing altitudinal data distributions of CG. Optimal bandwidth was chosen based on Silvermans rule (Silverman, 1986; Scott, 1992; Salgado-Ugarte et al., 1993). This statistical method was proposed by Rosenblatt (1956) and is defined as: Where,

h = bandwidth Xi = altitude value of each grid point K = Kernel function A kernel Gaussian function was used:

K(z) =
Where,

1 2

exp

z2 2

Z=

( x Xi) h

Optimal bandwidth was chosen based on Silvermans rule (Silverman, 1986; Salgado-Ugarte, 1995, 1997):

h=
Where,

0 .9 A n
1/ 5

A = min

( Xi x )2 1/ 2 Dispertion , n 1 1.349

Given that altitudinal data distributions were multimodal, we determined the dominant Gaussian components of each CG with Bhattacharyas semi-graphical method (1967) by using the programs presented by Salgado-Ugarte et al. (1994, 2005) for the statistical package Stata software 9.0 (Stata Corporation, 2005). There are four steps in Bhattacharyas method. First, the logarithmic differences of successive frequencies are calculated. Second, these differences are plotted and the components are selected by eye. This step is the graphical part of the method. Third, the line segment corresponding to each segment is estimated. Bhattacharya develops formulas for estimating the parameters of each componentthe mean, standard deviation, and frequency or proportion of the sample due to each componentfrom the angles and intercepts described by the negatively sloped line segments. Finally, an estimated frequency polygon is generated by adding the estimates of each of the Gaussian components (Salgado-Ugarte et al., 1994; Salgado-Ugarte et al., 2005). Once we obtained the dominant Gaussian components, we made a non-parametric analysis of variance Kruskal-Wallis with a post-hoc Z test to compare the medians of the Gaussian components to determine differences in altitude between CG of A. c. costata due to global warming. This contribution intends to introduce an alternative way to analyze one of the consistent responses of animals and plants in the face of global warming, i.e., moving to higher altitudes.

RESULTS Selection of climatic groups With the classification of the bioclimatic profile we found three groups (A, B, and C), mainly based on different climatic preferences (Fig. 1). The discriminant function analysis and the Mahalanobis distances corroborated with these CG across the geographical range of A. c. costata (Wilkis Lambda = 0.0457, F = 21.240, P < 0.0001, Table 1). Modeling method The number of variables selected for modeling the impact of climate changes on CG distributions was reduced from the original 22 variables (19 bioclimatic and three topographic data) to 14 variables (Table 2). According with PCA results, CG-C inhabits in the highest altitude in contrast CG-A and CG-B. The mean altitude is 2291 396.37 m (range: 11012927 m). This area has a cold and dry climate,

f (x) = density estimation for variable x

n = inspection number

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the annual mean temperature is around 15C and the mean annual precipitation is 700 mm (range: 3901052 mm) unlike CGA and CG-B, which inhabit warmer and wetter climates. The CG-A population lives in the warmest zone with an environmental temperature of 23C (15.627.6C) as distinguished from CG-B and CG-C. The mean altitude of the habitat of CG-A is of 1362.78 288.53 m (range: 1993621 m), and the mean annual precipitation is of 890 mm (range: 5781294 mm). Finally, CG-B inhabits a wetter climate. The mean annual precipitation is of 1006 mm (range: 696 1442 mm) and the mean annual temperature is of 22C (16.226.4C). This CG occupies a region with a lowest mean altitude: 1217.03 466.75 m (range 1132484 m). These temperature and precipitation differentiations affected daily activity periods, reproductive performance and behavior of lizards: for CG-A and CG-B the daily activity period is from 0800 h to 1800 h and the reproductive period is extended across seven months, but in CG-C, the scenario is very different, the daily activity period is from 1200 h to 1600 h, and the reproducFig. 1. Climatic groups of Aspidoscelis costata costata selected based on different clitive period is shorter (four months) than in matic preferences. Points indicate species records that were gathered from national and the other groups (personal observation). In international museum collections and some related references. Circles represent Climatic Table 3 we described a brief summary of group A, rectangles correspond to Climatic group B and triangles represent Climatic PCA results showing the difference in cligroup C. mate preference among the three CG populations. CG-A and CG-B had 66 and 76 records, respectively. We used 33 Table 1. Mahalanobis Distances between climatic groups of Aspidoscelis costata costata. points of CG-A and 38 of CG-B to construct an ecological niche model, and Squared Mahalanobis Distances F-values; df = 13,143 p-levels the rest were used to test the model. Climatic Climatic Climatic A B C A B C A B C On the other hand, we assigned 100% Group Group Group of the point localities for the training A 0 5.93 41.74 A 14.65 36.1 A 1.75E-20 0 data set for CG-C as it had only 16 B 5.93 0 43.46 B 14.65 38.55 B 1.75E-20 0 records. Results generated for each C 41.74 43.46 0 C 36.1 38.55 C 0 0 CG of A. c. costata had AUC values > 0.9 implying potentially significant results: CG-A (AUC = 0.992), CG-B Table 2. PCA 14 refers to the contribution of the first, second, third, and four PCA axes in (AUC = 0.992) and CG-C (AUC = explaining the cumulative percentage variation in climate variables on Aspidoscelis costata 0.990). This predictive ability is costata distribution. The selected variables are: [1] annual mean temperature, [5] max temperobserved in the zero omission error ature of warmest month, [6] min temperature of coldest month, [8] mean temperature of wettest registered in the models for three CG, quarter, [9] mean temperature of driest quarter, [10] mean temperature of warmest quarter, [11] as well as the fact that the areas mean temperature of coldest quarter, [12] annual precipitation, [13] precipitation of wettest obtained for the current distribution do month, [14] precipitation of driest month, [15] precipitation seasonality, [16] precipitation of wetnot show high overprediction, as comtest quarter, [18] precipitation of warmest quarter, and aspect (direction to which a mountain pared to known distribution. slope faces).
Eigen values PCA 1 PCA 2 PCA 3 PCA 4 9.85 4.81 2.31 1.78 Percentage 42.84 20.95 10.07 7.77 Cumulative Percentage 42.84 63.78 73.86 81.63 Selected variables 1, 10, 11, 14, 15, 5, 6, 8, 9 12, 13, 16 18 aspect

Future potential distribution Our modeling using MaxEnt projected potential shifts in the distribution areas of A. c. costata as a consequence of the climate changes represented by the CGCM2SRES A2 sce-

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Table 3. Mean and standard deviation values of the main bioclimatic parameters selected from the PCA analysis that were the most important variables predictors of Aspidoscelis costata costata habitat distribution.
Bioclimatic parameters Mean SD Max-Min Mean SD 23.2 2.4 25.4 2.6 21.1 2.2 1006.7 186.5 216.4 39.2 3.0 1.8 103.5 3.3 618.7 118.1 233.9 77.7 28.8 8.3 12.4 2.3 22.0 2.1 23.5 2.4 22.3 2.7 15132 11639.6 Max-Min Mean SD Max-Min

Climatic Group A 26.416.2 29.518.1 2413.9 1294578 268150 111 11287 715302 361187 9312 14.64.3 26.419.8 26.416.7 27.214.8 33343 1

Climatic Group B 27.615.6 30.617.6 25.213.2 1442696 333149 101 11391 926422 37855 5415 16.14.4 2618.9 27.216.4 28.413.2 35948 1

Climatic Group C 15.5 2.3 22.112.4 17.4 2.4 24.614 12.9 2.3 19.310.1 726.9 178.8 1052390 138.9 33.7 19776 7.1 4.2 224 84.3 7.2 9569 389.1 112.2 586166 244.7 48.6 335145 27.4 15.4 8317 4.4 2.3 112.1 22.2 0.9 23.219.7 16.8 2.2 23.213.4 13.2 2.5 20.610.1 15769 7041 346627469

Bio1 = Annual Mean Temperature (C) 22.3 2.2 Bio10 = Mean Temperature of Warmest Quarter (C) 24.5 2.5 Bio11 = Mean Temperature of Coldest Quarter (C) 20.1 2.0 Bio12 = Annual Precipitation (mm) 890.6 111.9 Bio13 = Precipitation of Wettest Month (mm) 194.7 20.8 Bio14 = Precipitation of Driest Month (mm) 3.3 1.4 Bio15 = Precipitation Seasonality (Coefficient of variation) 102.1 4.4 Bio16 = Precipitation of Wettest Quarter (mm) 528.9 77.4 Bio18 = Precipitation of Warmest Quarter (mm) 272.1 23.8 Bio19 = Precipitation of Coldest Quarter (mm) 26.7 10.8 Bio5 = Maximum Temperature of Warmest Month (C) 10.7 2.01 Bio6 = Minimum Temperature of Coldest Month (C) 23.2 1.6 Bio8 = Mean Temperature of Wettest Quarter (C) 23.1 2.2 Bio9 = Mean Temperature of Driest Quarter (C) 21.1 2.5 Aspect = Direction to which a mountain slope faces (meters) 19272.3 7057

Fig. 2. Potential distributions models of Aspidoscelis costata costata for liberal climate change scenario (SRES A2). Climatic group A for the years: (A) 2020, (B) 2050, and (C) 2080. Climatic group B for the years: (D) 2020, (E) 2050 and (F) 2080. Climatic group C for the years: (G) 2020, (H) 2050 and (I) 2080. Colors indicate the following: red = areas preserved in the future; blue = distributional areas lost; and green = new predicted distributional areas in the future.

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nario in the years 2020, 2050, and 2080 (Fig. 2). For CG-A the current potential distributional area was 315, 332 km2, which will be reduced to 254,075 km2 by 2080, conserving more than 80% of its modeled range (Fig. 2A, 2B, and 2C). For CG-B, the forecast current potential distributional area was 158,923 km2, which will be reduced by 47% in year 2080; but it could gain more than 31% (50,119 km2) of its area by the same year (Fig. 2D, 2E, and 2F). The picture looks even more severe for CG-C since the range will be reduced by 52% (from 113,899 km2 to 54,525 km2) of their potential current range and it could gain only 3% (3,289 km2) by 2008 (Fig. 2G, 2H and 2I).

Altitudinal variation The violin plots indicate that the environmental niches of the three CG of A. c. costata show a tendency toward an upward shift in response to climate warming toward 2080, which means that these reptiles may be able to move to higher altitudes. For CG-A and CG-B, the environmental niche showed an increase of more than 100 m in mean altitude toward 2080 (115.51 and 107.9 m, respectively) (Fig. 3A and 3B, respectively), whereas for CG-C the expansion was of 215.63 m (Fig. 3C). The results of the violin plots were supported by the extract of dominant Gaussian components of altitudinal data determined by the Bhattacharyas method. The results of the Gaussian components showed changes in the mean altitude of the three CG (Fig. 4). The Kruskal-Wallis analysis showed that these differences were statistically significant: CG-A (H3 = 49980.6, N = 188694, P = 0.000); CG-B (H3 = 37452.41, N = 81237, P = 0.000) and CG-C (H3 = 122590.4, N = 199257, P = 0.000) (Table 4). In our view the frequency of occurrence of individuals at certain altitudes reflects their tolerance limits, which are the indirect relations of histograms with bio-ecological processes. We used the most efficient methods to study the frequency, that is, the kernel density estimators (EDK), which can resolve some of the problems of the traditional histogram (specially the origin and discontinuity) (Silverman, 1986; Fox, 1990). The resulting density estimators also exhibit complex distribution. One approach to resolve such

Table 4. Results of the multiple comparison post-hoc Z test for the three climatic groups of Aspidoscelis costata costata. Numbers in bold show those periods of time that are different. Climatic Group Current Potential Distribution 2020 A 2050 2080 Current Potential Distribution 2020 B 2050 2080 Current Potential Distribution Fig. 3. Violin plots that show altitudinal data distributions for climatic groups of Aspidoscelis costata costata: (A) Climatic Group A, (B) Climatic Group B and (C) Climatic Group C. Ends of boxes are the 25th and 75th quartiles; interquartile range is the difference between quartiles; lines across middles of boxes are medians; while the line at each side of the box plot is the kernel density plot. 2020 C 2050 2080 4.65 0.00 194.38 0.00 300.55 0.00 1.33 1 2.06 0.24 167.63 0.00 223.49 0.00 6.48 0.00 6.55 0.00 Current Potential Distribution 2020 223.49 0.00 2050 6.48 0.00 0.04 1 2080 6.55 0.00 0.11 1 0.05 1

0.04 1 0.11 1 1.33 1

3.28 0.01 162.42 0.00 4.65 0.00

178.93 0.00 283.63 0.00

0.05 1 2.06 167.63 0.24 0.00 3.28 162.42 0.01 0.00 163.39 0.00 163.39 0.00 194.38 300.55 0.00 0.00 178.93 283.63 0.00 0.00 155.91 0.00 155.91 0.00

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complex frequency behavior is to consider the distribution as a mix of individual components. As a first step, from those mixed distributions we extracted the component with the high-density (frequency) value considered as a dominant component. This component contains an important fraction of the total frequency distribution and may be used as an indicator of the relation with ecological and biological characteristics of the species involved. DISCUSSION We provide here the first comprehensive study on the potential effect of global warming on the geographic distribution of a teiid lizard. The results of this study shows the potential distribution area of three CG of A. c. costata will experience in some cases significant reductions and in others important expansions by the year 2080 due to global warming. According to the literature, warming in low latitudes and altitudes will be relatively small in magnitude. However, in these regions, warming will likely have the most deleterious consequences, as organisms are currently living very close to their optimal temperature (Deutsch et al., 2008). In contrast, species at higher latitudes and altitudes have broader thermal tolerance and are living in climates that are currently cooler than their physi-

Fig. 4. Graphics indicating dominant Gaussian components estimated for altitudinal data for: 1) Climatic Group A, 2) Climatic Group B and 3) Climatic Group C of Aspidoscelis costata costata. (A) Current altitudinal distribution, and future altitudinal potential distribution for (B) 2020, (C) 2050 and (D) 2080. Numbers in the right corner of each figure show the mean and the standard deviation (x SD) of the dominant Gaussian component. The line with circles represents the observed frequencies and the lines with dots correspond to the dominant Gaussian component.

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ological optima, indicating that warming may even enhance their fitness (Addo-Bediako et al., 2000; Ghalambor et al., 2006). Beyond latitude and altitude considerations, ecological habitats need also to be considered. CG-A and CG-B inhabit a region dominated by tropical dry forest. According to Villers-Ruiz and Trejo-Vzquez (2004), this type of vegetation could expand its distributional area to higher altitudes in response to global warming. However, the same authors explain that this ecosystem has had the most deleterious damage due to anthropogenic activities. Therefore, the synergetic effect of habitat destruction with global warming could be more devastating for CG-A and CG-B of A. c. costata, since these CG inhabit one of the most degraded and populated regions of Mexico. The CG-C population has the bleakest prognosis. This group inhabits pine forest remnants. This vegetation type does not tolerate a rise in environmental temperature; therefore it is likely to disappear due to actual global warming (Villers-Ruiz and Trejo-Vzquez, 2004). As a result, MaxEnt forecasted a loss of more than 50% of its current potential distribution, and a gain of only 3% by year 2080. We must be able to accurately predict range shifts in order to mitigate impacts on biodiversity and propose appropriate conservation strategies. What is usually overlooked in these modeling efforts is the fact that species can be composed of different populations or geographical groups across their ranges, which have the potential to respond independently to changes in climate (Arajo et al., 2006). In this sense, our results draw attention to the importance of modeling climatic or geographic groups and/or populations instead of the entire species range treated as a homogeneous entity. In other respects, our results showed an altitudinal shift among CG of A. c. costata, which agrees with the results found in species of insects (Parmesan et al., 1999; Deutsch et al., 2008), birds (Thomas and Lennon, 1999), mammals (Hersteinsson and MacDonald, 1992) and plants (Hansen et al., 2001). These modifications can induce alterations in community structure and in the relative abundance of species, as well as increases in habitat fragmentation and population extinction (Davis et al., 1998; Peterson et al., 2002). At present Aspidoscelis species have some problems that need to be overcome if they want to reach higher altitudes. The first one is to attain and maintain a high body temperature (i.e. 40C, Vitt and Pianka, 2004). The second challenge that A. c. costata must confront involves female reproductive physiology. Females of this genus typically keep their eggs inside oviducts for short periods of time from seven to 20 days (McCoy and Hoddenbach, 1966; Christiansen, 1971) to avoid the negative effects of high body temperature during gestation. As a result, a major portion of embryonic development occurs out at the nesting site making this species especially vulnerable to global warming. But according with our results, the distribution of the environmental requirements of the ecological niche for the presence of A. c. costata will expand to higher altitudes due to global warming, which means that this lizard will not have problems to reach higher altitudes, as the environmental requirements needed for survival today will be present at higher altitudes in the future.

In the present study, we developed a method to evaluate the potential altitudinal distribution under a climate change scenario for A. c. costata. As an exploratory tool we used a violin plot, which helped us to determine the structure found within altitudinal data. The components of these violin plots comprise a box plot and a kernel density plot (Hintze and Nelson, 1998). Although the box and whiskers diagrams are very useful graphs, their construction is only based on five values (and some derivative ones): median, quartiles, and extremes and in spite of may give an adequate indication of skewness and outliers, they do not give any glimpse of multimodality, as is the case of the distributions obtained in this work. For this reason, we used a kernel density estimator, which is considered to be among the best distribution descriptors available, as they are improved histograms (Silverman, 1986). Besides, the resulting density estimators exhibit complex distribution, not a simple Gaussian (normal) distribution or an asymmetric (biased) one. The distribution had several regions of point concentration (several levels) which means that coexist several (simpler) individual components (mixed distribution). Therefore in order to understand the complex distribution of altitudinal data we identified the dominant component (as a single Gaussian distribution), as it contains an important fraction (and often the main part) of the information regarding the behavior of the studied phenomenon (Salgado-Ugarte et al., 1994). Because the impact of warming will be both site- and species-specific, and biotic interactions directly influence energy gain and fitness much work remains to be done to identify the magnitude and consequences in A. c. costata persistence due to global warming. ACKNOWLEDGMENTS
We thank the Instituto de Biologa and Posgrado en Ciencias Biolgicas of Universidad Nacional Autnoma de Mxico. We also thank Consejo Nacional de Ciencia y Tecnologa for graduate study scholarships to MAGR (CONACYT no. 165072). This article is a requisite for MAGR to obtain a Ph.D. degree within the Posgrado en Ciencias Biolgicas of Universidad Nacional Autnoma de Mxico. Special thanks to Constantino Gonzlez Salazar for his help during the development of this work. We thank the California Academy of Science Herpetology Collection Catalog (CAS), the Illinois Natural History Survey (UIMNH), the Los Angeles County Museum of Natural History (LACM), Michigan State University Museum (MSUM), Museum of Natural Science (LSU), Museum of Southwestern Biology of the University of New Mexico (MSB), National Museum of Natural History Smithsonian Institution (USNM), Texas Cooperative Wildlife Collection-Herpetology Collection (TCWC), University of Kansas Biodiversity Research Center Herpetology Collection (UK), University of Arizona Museum of Natural History (UAZ), Coleccin Nacional de Anfibios y Reptiles del Instituto de Biologa, UNAM (CNAR-IBH), Museo de Zoologa de la Facultad de Ciencias, UNAM (MZFC), British Museum of Natural History (BMNH), American Museum of Natural History (AMNH), Arizona State University (ASU), Brigham Young University (BYU), Carnegie Museum of Natural History (CM), University of Colorado Museum (UCM), Field Museum of Natural History (FMNH), Collection of Herpetology, University of California, Los Angeles (MVZ), University of Michigan Museum of Zoology (UMMZ), Sistema Nacional de Informacin Biolgica-CONABIO (SNIB), and Escuela Nacional de Ciencias Biolgicas del Instituto Politcnico Nacional (ENCBIP) for species records.

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