Effect of climate change on halophytic grasslands loss and its impact in the viability of Gopherus flavomarginatus

The decrease of the habitat is one of the main factors that affect the survival of G. flavomarginatus. This study assesses the halophytic grasslands loss over a period of 30 years in the distribution area of the Bolson tortoise and the effects of climate change on the habitat suitability of these grasslands and its possible impact on this tortoise. Grassland loss was assessed by an analysis of symmetric differences and the habitat suitability model was carried out by the method of overlapping layers raster. Our results showed a grassland loss of 63.7%; however, our current habitat suitability model points out that much of the grassland loss has occurred where the environmental conditions are suitable. These results suggest that anthropic activity is a main factor in the habitat disturbance in the study area. Likewise, the models for years 2050 and 2070 under the criteria RCP 2.6, RCP 4.5, RCP 6.0, suggest that anthropic activity will continue be the main cause of the grassland loss. Therefore, considering the association between the Bolson tortoise and grassland halophyte Hilaria mutica, which comprises around 60% of its diet, the viability of the Bolson tortoise depends largely on strategies aimed at protecting the soil that allow the presence of this grassland.


Introduction
Climate influences plant and animal distributions due to their requirements related to temperature and humidity (Parmesan and Yohe 2003;Root et al. 2005;Walther et al. 2005;Lavergne et al. 2006).It has been documented that when climatic factors are extreme, these can exceed the level of tolerance of species, preventing the optimal expression of their life cycles (Gutiérrez and Trejo 2014).Each species has a tolerance interval to diverse environmental factors (Walther et al. 2002;Hardy 2003;Dawson and Spannagle 2009); therefore, its distribution depends on their fundamental niche and their biological interactions (Pearman et al. 2008).
Climate change and change of land use are two of the factors that most affect natural systems (Burroughs 2001;Shafer et al. 2001;Iverson et al. 2008;Harsch et al. 2009;IPCC 2014).The effect of the climate change is more severe on arid and semiarid ecosystems than on humid and semihumid ecosystems (Grime et al. 2008).Thereon, it has been mentioned that facing loss of vegetation of the arid zone, the presence and animal behavior that feed on desert plants could be modified, generating a decrease in the distribution area and in size of their populations (Gandiwa and Zisadza 2010).The effects of the transformation of the vegetation, however, are not uniform for all animal species (Fahrig 2003).Species' response to environmental change will be determined by their physiology (climatic tolerance), morphology (i.e., body size), ecology (feeding habits, habitat selection; nesting sites), dispersal capacity and behavioral characteristics (foraging time, general activity).Therefore, there are species with negative responses by decreasing its abundance and/or its distribution, as well local extinction (Midgley et al. 2007), and other species with positive responses reflected in increasing their abundance and expanding their distribution (Stotz et al. 1996;Thomas et al. 2004;Moritz et al. 2008;Lara et al. 2012).
To assess the effect of the climate change on species distribution, ecological niche modeling has been used employing different environmental variables and mathematical algorithms that try to simulate the climate niche of a species and represent it geographically on a map (Parmesan 2006;Mckenney et al. 2007).In most of the studies, on large spatial scales, only climatic variables have been used for predicting spatial distribution of the species (Araújo and Peterson 2012;Anadón et al. 2015).In some cases, dealing with local spatial scales, soil and orography variables have been included (Guisan and Hofer 2003;Pearson et al. 2004;Anadón et al. 2007;Marini et al. 2010;Kreakie et al. 2012), for example, the dependence of herbivores specialized on some plants (Kissling et al. 2007).Nevertheless, it is very difficult to determine spatial data of biological interactions; and for this reason the studies where the interactions are used to assess the distribution area of the species are very scarce (Pearson and Dawson 2003).
Chihuahuan Desert grasslands provide important resources as habitats and food for sustaining a very rich animal diversity (Vickery et al. 1999).However, the degradation of grasslands is one of the main causes of biodiversity loss on a global scale  (Gavilán 2008).Given this situation, endemic or native species are the most vulnerable (Contreras-Balderas et al. 2003).Gopherus flavomarginatus is an endemic tortoise species of the Bolson of Mapimí zone of the Chihuahuan Desert in the north-central México (Figure 1).The Bolson tortoise is considered vulnerable by IUCN Red List (2017).This species inhabits halophytic grasslands of Hilaria mutica on which it feeds, presenting an apparently mandatory association (Aguirre et al. 1979).Therefore, there exists a close interaction between the presence of the grassland and that of the tortoise.
Historically, the Bolson tortoise was distributed from the southwestern USA to the center of México.However, it is currently confined to the area known as the Bolson of Mapimí (Lemos-Espinal and Smith 2007).Considering the low dispersal capacity of the Bolson tortoise and its dependence on the halophytic grass H. mutica, a reduction of this grassland, brought about by climate change in the Bolson of Mapimí, would be expected having a strong impact on the viability of the tortoise.Therefore, the goals of this study are: (i) to estimate the change in halophytic grasslands from 1980-2013 period on the current distribution range of G. flavomarginatus, (ii) to estimate the projected effect of climate change for the years 2050 and 2070 on the distribution of halophytic grasslands in the Chihuahuan Desert, and (iii) to assess the possible impact of the halophytic grasslands changes on the viability of G. flavomarginatus.

Study area
The Chihuahuan Desert has an approximate area of 507,000 km 2 and elevations from 800 to 2500 m-asl; it extends from central México northward to southern Texas, Arizona, and New México.The mean annual precipitation varies from 175 to 400 mm.The characteristic vegetation is microphyllous desert scrub, rosette desert scrub, crassicaule desert scrub, and grasslands, among others (Rzedowski 1978).About 80% of the soils are derived from calcareous materials (Sutton 2000).Halophytic grasslands of H. mutica are distributed throughout the Chihuahuan Desert, whereas the tortoise occurs only in the central zone, in the region known as Bolson of Mapimí, where the Mapimí Biosphere Reserve is located (Lemos-Espinal and Smith 2007).

Zonification of the distribution area of the Bolson tortoise
Sixty one records of G. flavomarginatus were identified, with these points we delimited a Minimum Convex Polygon (MCP) of 15,895.5 km 2 that represents the distributional area of the Bolson tortoise.This polygon was zoned according to the densities of the geographic points using the clustering K-means method (Software CrimeStat V. 3.2, 2009).

Influence of the environmental factors on distribution of halophytic grassland
In order to identify loss and gain areas of halophilic grasslands  we used a symmetric difference analysis (Software ArcMap V. 10.1; ESRI 2012).The analysis was performed by using a quadrant of 32,300 km 2 (MCP2) product of add a buffer zone of 10 km around the perimeter of MCP.To this quadrant was added information of land use and vegetation distribution (INEGI 1991(INEGI , 2013)).Likewise, we provided current environmental data (19 climatic layers) with a spatial resolution of 2.5 minutes (~5 km 2 ), obtained from Worldclim (Hijmans et al. 2005); The bioclimatic variables of Worldclim reflect aspects of temperature and precipitation and have been used successfully for niche models (Davis et al. 2008;Jezkova et al. 2009).
Subsequently, within the area MCP2 were settled 232 quadrants out of 100 km 2 , each one.In each quadrant we added the corresponding value for each bioclimatic variable, as well as the information of presence and absence of the halophytic grasslands.In order to identify the bioclimatic variables that explain the presence and absence of the halophytic grasslands in the study area, was used an analysis of discriminant factors (canonical) under the generalized linear model.This analysis was performed using the library "MASS" (Venables and Ripley 2002) in the software R (version 3.1.3).

Habitat suitability models
For modeling the habitat suitability of halophytic grasslands under current climatic conditions in the Chihuahuan Desert, we used the retained bioclimatic variables in the discriminant analysis.The selected variables were annual mean temperature, mean diurnal range, minimum temperature of the coldest month, annual precipitation, and precipitation of wettest quarter, as well as substrate texture data (INEGI 2004).Based on these variables we performed an analysis of frequencies with the purpose of obtaining the climatic profile (maximum and minimum) of the halophytic grasslands.Later, the habitat suitability was modeled using an Additive Overlay Analysis of layer raster method (ArcMap V. 10.1), which delimits the potential habitat suitability of one species based on knowledge of its climatic profile.To these are given a weighting according to the importance of the layer and abundance of the points on the polygon, and the cells are extracted from the raster layer by a logical search.Outlet layers contain only the values of the cells or pixels extracted from the input layer and output layers that were used in the superposition processes.
The same climatic profile was used for modeling habitat suitability for the scenario of the climatic change to 2050 and 2070 in the Chihuahuan Desert.We used data as scenarios of the climatic change corresponding to the extrapolated with Beijing Climate Center Climate System Model (BCC-CSM1-1, this was chosen at random from a group of 19 climate models) for the years 2050 and 2070 under different Representative Concentration Pathways (RCP): RCP 2.6 = +2.6W/m 2 , RCP 4.5 = +4.5 W/m 2 , RCP 6.0 = +6.0W/m 2 , and RCP 8.5 = +8.5 W/m 2 were used as scenarios of the climatic change.Under the scenario RCP 2.6 a minor intensity of the effects of the climate changes is expected, while with the scenario RCP 8.5 the intensity will be greater (Weyant et al. 2009).The model additive overlay of layer raster predict habitat suitability as a function of environmental variables and species occurrence data, this habitat suitability is represented by a scale ranging from 0 (low suitability) to one (high fitness), we used a cut-off point of 0.5.
The emergence of new technologies and recent assumptions about socioeconomic development, as well as observations of environmental factors such as land use and land cover change have been considered in this new generation of scenarios (Moss et al. 2010;Rogelj et al. 2012;van Vuuren 2012).The RCPs explicitly explore the impact of different climate policies in addition to the no-climate-policy SRES scenarios (van Vuuren et al. 2011b) and provide an important reference point to investigate the potential implications of climate change on ecosystems (van Vuuren et al. 2011a).
For the validation of the model were used the zones with presence of halophytic grasslands in the Chihuahuan Desert reported by the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (CONABIO) (2015).

Exchange rate
To assess the climate change impact on the habitat suitability of the halophytic grasslands we obtained the percentage change for each scenario using the following formula (Gutiérrez and Trejo 2014): Where: S0, is the total surface of the study area, according to the base scenario.S1, is the total surface occupied in the study area under change conditions.

Results
Three zones in the distribution area of G. flavomarginatus were identified, these zones were classified as "A" with 2,649.99 km 2 , "B" with 5,472.21km 2 , and "C" with 2,657.11km 2 (Figure 2).The zone "A" coincides with the polygon of the Reserve of Mapimí Biosphere, and it is the lesser extension of the three identified zones (Figure 2).For MCP2 (quadrant of 32,300 km 2 ), in a period of 30 yrs, we recorded a halophytic grasslands loss of 1,286.66km 2 and a gain of 518 km 2 (Figure 2); therefore, for the year 2013 the extension of the halophytic grasslands in the MCP2 was 1350.44 Km 2 .The transformed Wilks value, obtained from discriminant analysis shows that the null hypothesis should be rejected (λ = 0.834, x 2 = 56.478,g.l.= 18, p = 0.000); therefore, the two discriminant groups (presence and absence) should be considered as distinct.
The current model habitat suitability identifies the greatest part of the localities where halophytic grasslands had been reported in the Chihuahuan Desert (CONABIO 2015) (Table 1, Figure 3); the projected habitat suitability for Chihuahuan Desert shows that habitat suitability loss was relatively low for the scenarios RCP 6.0, RCP 4.5, and RCP 6.0 for the years 2050 and 2070 (Table 2, Figure 3).However, under the scenario RCP 8.5 for the years 2050 and 2070 the models of habitat suitability show a loss of 43.18% and 89.3%, respectively.Considering the scenario RCP 8.5 for year 2050, halophytic grasslands only it remains in B zone; while for year 2070 disappear completely the habitat suitability in the current distribution area of the Bolson tortoise (Table 2, Figure 3).Under the scenario RCP 8.5 for 2050 and 2070, the loss of habitat suitability for halophytic grassland was much higher than for the rest of the scenarios (Table 2).In RCP 2.6 we obtained the lower estimates of reductions of habitat suitability for grasslands.

Discussion
The results of this study show that halophytic grassland loss in the current distribution area of G. flavomarginatus has been a continuous process, in as much as in a period of Figure 2. Distribution of gain and loss of the halophytic grassland in an area of 32,300 km 2 .Black spots show populations of G. flavomarginatus; dotted lines show distribution zones "A", "B" and "C" of the species; the black line indicates the Mapimí Biosphere Reserve; dark grey color shows the zones with gain of halophytic grassland; light grey color shows the zones of halophytic grassland loss; medium grey color shows areas with grasslands that has been maintained; the grid make reference to squares of 100 km 2 in the study area.30 years its reduction has been 63.7%, with the zone "A" being the most affected.In this context, halophytic grasslands loss for the Chihuahuan Desert has been attributed to the climatic change and to the anthropic factors (e.g., agriculture and cattle; Vavra et al. 1994;Archer et al. 1995;Hodgson and Illius 1996;Aguirre et al. 1997; Moleele  and Perkins 1998;Van Auken 2000).In this regard, Archer (1994) pointed out that the grassland loss is an event that is happening in arid and semiarid ecosystems worldwide; while Comstock and Ehleringer (1992) and Cook and Irwin (1992) showed that the climate is the main factor to explain the variation in vegetation patterns.
The current habitat suitability model of this study indicates that climatic conditions of the area that showed the highest loss of halophytic grassland inside the known distribution range of G. flavomarginatus (zone "A") are appropriate for the presence of this grassland.Data on land use and vegetation presented by Instituto Nacional de Estadística y Geografía (INEGI 2013) show that zone "A" and its surroundings presents a strong agricultural and cattle impact.Likewise, it has been noted that reduction and fragmentation of the vegetation cover in the Natural Protected Area of Mapimí Biosphere placed inside Zone "A" is caused by overgrazing (CONANP 2006).In this manner, based on this information, it is possible to point out that beyond the influence of the environmental factors in determining the presence or absence of halophytic grassland, anthropic activities are the main factors that are influencing the loss of this grassland in the current distribution area of the Bolson tortoise by causing fragmentation of this corridor route of halophytic grassland among zones A, B, and C.
In this context, it has been documented that changes in vegetal species distribution promote that animal species also modify their behavior and distribution (Gurd et al. 2001;Steffan-Dewenter et al. 2002).However, when individuals of one species are not able to disperse and colonize new areas with suitable habitat quality or do not possess a wide range of physiological tolerance, their extinction is highly likely (Holt 1990;Kattan and Murcia 2003;Brooks et al. 2004;Uezu et al. 2005;Wilcox and Thurow 2006).In this regard, it has been pointed out that this situation is frequently observed in specialist species (Gascon et al. 1999).For example, it has been documented that grassland fragmentation in the Chihuahuan Desert has affected the biological biodiversity causing isolation and reduction in 60% of the bird populations that inhabit grasslands (Desmond et al. 2005).Likewise, in Cynomys mexicanus, an endangered mammal and strongly associated with halophytic grassland in the Chihuahuan Desert, it has been seen that the distance among colonies of this species increase with the grassland fragmentation preventing natural dispersal and the interactions of the animals among populations (Yeaton and Flores-Flores 2006).
For the lizard species Uma exul and Uma paraphygas, it has been reported that their specificity on dune ecosystems and their low dispersal capacity reduce the probability of migration to places where the habitat conditions are suitable to live.These two species show very low genetic variability; therefore, it has been pointed out that these species are in critical condition because of the transformation of their habitat (Gadsden et al. 1993;Gadsden 1997;Ballesteros-Barrera et al. 2007).Likewise, since 1987, in 20 of 50 amphibian species of cloud forest from Monte Verde, Costa Rica, including the endemic Golden Frog (Incilius periglenes), as well as species of the Anolis genus have disappeared because of habitat fragmentation (Schneider 1999).
Accordingly, considering the association between Bolson tortoise and the halophytic grass H. mutica that comprises 60% of its diet (Aguirre et al. 1979), and taking into account the decreased food availability in the environment, the Bolson tortoise tends to reduce its home range (Hoogland 2006).Therefore, its low dispersal ability (Ureña-Aranda et al. 2015), low genetic variability (Ureña-Aranda and Espinosa de los Monteros 2012), and fragmentation and loss of grassland H. mutica are the main threats for the Bolson tortoise, because these factors favor isolation of the populations of this tortoise by intensifying the low genetic variability of the species.These conditions promote less resistance to extreme temperatures, drought events, change in food availability, emerging diseases, among other features, thus causing population extinction (Hoelzel et al. 2002;Russello et al. 2004;Zhang et al. 2004).
On the other hand, expectations of climate change for years 2050 and 2070 under scenarios RCP 2.6, RCP 4.5, and RCP 6.0 show a slight decrease in habitat availability for halophytic grassland in the Chihuahuan Desert, zones A and B, however show relative stability.This suggests that fragmentation of halophytic grassland in the range of the Bolson tortoise will depend on the change in land use.Under conditions of a pessimistic scenario (RCP 8.5) change rate of the habitat suitability area for halophytic grassland in the Chihuahuan Desert for years 2050 and 2070 will be of -45.186 and -81.333%, respectively.Under this scenario the viability of the Bolson tortoise is heavily compromised.
In conclusion, viability of the Bolson tortoise will depend on the strategies of protection and the land conservation allowing for the presence of halophytic grassland composed of H. mutica.In this regard, conservation programs for the Bolson tortoise and its habitat currently are addressed mainly within the Mapimí Biosphere Reserve; however, according to the available evidence, this zone is strongly affected by anthropogenic factors.Likewise, monitoring programs of the populations and habitat conditions of the Bolson tortoise are performed in an area of 1 km 2 scattered inside the Protected Natural Area (CONANP 2016).Faced with this situation, conservation programs of the habitat are needed for allowing connection of the populations inside and outside the Protected Natural Area.Therefore, we propose protection of the A, B, and C zones and the connections among them, so that in this way genetic interchange among populations can be favored.On the other hand, due to threats of climate change, it is necessary to develop an ex situ conservation program for G. flavomarginatus as well as the conservation of the area that show a habitat suitability outside the current distribution range of the Bolson tortoise, thinking about reintroduction of the species.Also, it is necessary to point out that the algorithms of potential area of habitat suitability involve a certain level of uncertainty that becomes worse in the projections to simulated scenarios (Pearson et al. 2006).However, we consider that our results provide an early warning about the possible consequences of the current activities on land use and the climate change due to increasing temperature.

Figure 3 .
Figure 3. Habitat suitability models of the halophytic grasslands projected for Chihuahuan Desert.White lines show states boundaries; black lines refer to the Mapimí Biosphere Reserve; blue lines indicate distribution zones of G. flavomarginatus.

Table 2 .
Change rate of the habitat suitability area for halophytic grassland in Chihuahuan Desert considering current and future climatic conditions (2050 and 2070) under concentrations of greenhouse gases RCP 2.6, RCP 4.5, RCP 6.0, and RCP 8.5.

Table 1 .
Habitat suitability for distribution of G. flavomarginatus considering the different climatic scenarios assessed.