ISSN 1827-9635 (print) © Firenze University Press ISSN 1827-9643 (online) www.fupress.com/ah Acta Herpetologica 6(1): 105-118, 2011 Climate change and peripheral populations: predictions for a relict Mediterranean viper José C. Brito1, Soumia Fahd2, Fernando Martínez-Freiría1, Pedro Tarroso1, Said Larbes3, Juan M. Pleguezuelos4, Xavier Santos5 1 CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Campus Agrário de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal. Corresponding author. E-mail: fmartinez_freiria@yahoo.es 2 Département de Biologie, Faculté des Sciences, Université Abdelmalek Essaâdi, Tétouan, Morocco. 3 Faculté des Sciences Biologiques et Agronomiques, Université M. Mammeri. Tizi-Ouzou, Algeria. 4 Departamento de Biología Animal, Facultad de Ciencias, Universidad de Granada, E-18071 Grana- da, Spain. 5 Departament de Biologia Animal, Universitat de Barcelona, Av. Diagonal 645, E-08028 Barcelona, Spain. Submitted on: 2010, 26th December; revised on 2011, 10th May; accepted on 2011, 26h May. Abstract. Ecological niche-based models were developed in peripheral populations of Vipera latastei in North Africa to: 1) identify environmental factors related to spe- cies occurrence; 2) identify present suitable areas; 3) estimate future areas according to forecasted scenarios of climate change; and 4) quantify habitat suitability changes between present and future climatic scenarios. Field observations were combined with environmental factors to derive an ensemble of predictions of species occur- rence. The resulting models were projected to the future North African environmen- tal scenarios. Species occurrence was most related to precipitation variation. Present suitable habitats were fragmented and ranged from coastal to mountain habitats, and the overall fragmented range suggests a relict distribution from wider past ranges. Future projections suggest a progressive decrease in suitable areas. The relation- ship with precipitation supports the current unsuitability of most North Africa for the species and predicts future increased extinction risk. Monitoring of population trends and full protection of mountain forests are key-targets for long-term conser- vation of African populations of this viper. Predicted trends may give indications about other peripheral populations of Palearctic vertebrates in North Africa which should be assessed in detail. Keywords. Climate change, conservation, Mediterranean, biogeography, range regression, Vipera latastei. mailto:fmartinez_freiria@yahoo.es 106 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos INTRODUCTION The complex geographic shifts around the Strait of Gibraltar over the past 14 million years (De Jong, 1998) resulted in high percentages of European and African species found in Morocco and Iberian Peninsula, respectively (Schleich et al., 1996; Sindaco and Jeremcen- ko, 2008). The Pleistocene climatic oscillations have also produced shifts in species ranges (Hewitt, 2000): during cold periods, European species in North Africa expanded their range, but in warm periods, they have experienced severe reductions in the southern part of their range, with populations remaining isolated in mountainous areas (Santos et al., 2009). Currently, North-western Africa has the highest diversity and number of European- originated relicts of terrestrial reptiles in the Mediterranean Basin (Bons and Geniez, 1996; Schleich et al., 1996; Pleguezuelos et al., 2010). During the last 10,000 years, the region has been subjected to enormous landscape changes for both natural reasons (climate warming during the Holocene) and human activities (Charco, 1999). Presently, it is estimated that only 4.7% of the original Mediterranean forests remain (Cuttelod et al., 2008). Thus, many European taxa in North Africa are presently restricted to isolated mountains where suitable habitats endure (Bons and Geniez, 1996; Schleich et al., 1996). Range reductions and shifts to higher elevations are expected in mountain specialists (Peterson, 2003) and highlands may act as refuges against climatic constraints (Nogués-Bravo et al., 2007). Climate change scenarios for North Africa predict a decrease in rainfall of 10-200 mm by 2025 (Paeth and Thamm, 2007), which may increase the vulnerability of these populations to extinction. The Lataste’s viper, Vipera latastei, is an appropriate taxon to analyse potential effects of climate change in the extinction vulnerability of European-originated relicts in North- western Africa because: 1) it is a species of European origin that colonised North-west- ern Africa prior to the formation of the Strait of Gibraltar (Saint-Girons, 1980; authors, unpub. data); 2) the global distribution is well known (Brito et al., 2008); 3) several life- history traits, such as low growth rates, frequency of reproduction and dispersion capac- ity, and feeding specialisation, make it prone to local extinction (Brito and Rebelo, 2003; Pleguezuelos et al., 2007; Santos et al., 2007a); 4) the rare reported occurrences in North- western African, even in areas relatively well sampled (Bons and Geniez, 1996; Real et al., 1997; Fahd and Pleguezuelos, 2001), suggest low population densities; and 5) its dis- tribution is highly related to an environmental variable, the annual precipitation, at both regional and local scales (Brito et al., 2008; Martínez-Freiría et al., 2008). Populations of V. latastei in North Africa were ascribed to the subspecies V. l. gaditana (Saint-Girons, 1977). They have been shown to constitute morphologically dif- ferentiated groups (Brito et al., 2008) and genetical substructuring has been identified for Morocco and Algeria, probably related to the opening of the Gibraltar Strait (authors, unpub. data). African populations occur within a concise area, from the Rif and Mid- dle Atlas mountains of Morocco to western Tunisia, isolated by the Mediterranean from the remaining European populations. Previous biogeographical studies suggested that local environmental pressures are related with the African range of the species (Brito et al., 2008). These factors, combined with the Near-Threatened status in Morocco (Plegue- zuelos et al., 2010) and the rareness and fragmented character of the species in Africa, stress the need for the development of regional evaluations of species vulnerability to cli- mate change. Analyses within geographical limits are useful (Czech and Krausman, 1997) 107Climate change and relict viper populations because most decisions and budgets on the management of a species of conservation con- cern are planned independently by the different countries within the range of a species (Rodrigues and Gaston, 2002; Samways, 2003). This study uses ecological niche-based models in African relict populations of V. latastei to: 1) identify suitable areas for species occurrence in present time; 2) estimate future suitable areas according to forecasted scenarios of climate change; and 3) quan- tify habitat suitability changes between present and future climatic scenarios. We intend to provide insights on the vulnerability to extinction of European-originated relict taxa in North Africa to predicted climate change impacts. MATERIAL AND METHODS Data The study area comprises northern regions of Morocco, Algeria and Tunisia (Fig. 1). A total of 33 viper localities (Table 1) were collected from bibliographic records (Boettger, 1883; Dolfus and Beaurieux, 1928; Chpakowsky and Chnéour, 1953; Bons, 1958, 1963; Saint-Girons, 1977; Mediani et al., 2009), museum collections (MNHN Paris, MNCN Madrid, Univ. Salamanca), unpublished observations given to authors, and fieldwork conducted between 1989 and 2009 (Fahd and Plegue- zuelos, 2001; Fahd et al., 2005, 2007; authors, unpub. data). Fieldwork observations were georefer- enced to the GPS precision (WGS84 datum). Given the restricted range of microhabitats occupied by the species (Santos et al., 2006; Brito et al., 2008; Martínez-Freiría et al., 2008), bibliographic and museum localities were georeferenced with a precision of 1 × 1 km. Environmental factors, or ecogeographical variables (hereafter EGV), were selected according to their importance to the distribution of V. latastei (Santos et al., 2006; Brito et al., 2008; Martínez- Freiría et al., 2008): annual average temperature (ANTE), annual temperature range (TANR), maxi- mum temperature of warmest month (TMAX), annual precipitation (ANPR) (Hijmans et al., 2005), and one topographical grid (USGS, 2006) from which slope (SLOP) was derived with the Geographi- cal Information System (GIS) ArcGIS 9.2 (Table 2). Future climate data from three Global Circulation Models (GCM: CCCMA, HADCM3 and CSIRO) and two IPPC 3rd Assessment emission scenarios (A2a and B2a) for three time periods (2020-2050, 2050-2080 and 2080-2100) (IPCC-TGICA, 2007) Fig. 1. Location of the study area within the Mediterranean context, distribution of observations of Vipera latastei in North-western Africa and major toponomies in the study area. 108 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos were obtained from WorldClim (Hijmans et al., 2005). The resolution of EGVs was standardised to a grid cell size of 0.0110 degrees (about 1 × 1 km) for matching the resolution of observations. Analy- ses were developed using a geographic coordinate system given the limited latitudinal extent of the study area. Correlations between EGVs were relatively negligible (r < 0.599 in all cases). The presence sample size available for developing ecological models was very small which is mostly related to the rareness and localised character of the species in Africa (Bons and Geniez, 1996; Schleich et al., 1996) and sampling restrictions in politically unstable areas. These constraints Table 1. Location of observations of Vipera latastei used to develop the ecological models. The year and the origin of the observation are also included. Locality, Country Year Reference Oued Bou Regieg, Morocco 1959 Bons, 1963 Mamora forest, Morocco 2008 unpub. data given to authors Tanger, Morocco 1982 Boettger, 1883 Jbel Haouch Ben Lake’aa, Morocco 2009 Mediani et al., 2009 Astouf, Morocco 1990 Collection DBA Granada Jbel El Alem, Morocco 2000 authors, unpub. data Oued Laou, Morocco 1986 unpub. data given to authors Kelti, Morocco 2005 authors, unpub. data Ain Rami, Morocco 1992 Fahd and Pleguezuelos, 2001 Chaouen, Morocco 1992 Fahd and Pleguezuelos, 2001 Fifi, Morocco 2008 unpub. data given to authors Azrou, Morocco 1928 Dolfus and Beaurieux, 1928 Talassemtane, Morocco 2001 authors, unpub. data Bou Slimane, Morocco 1992 Fahd and Pleguezuelos, 2001 Béni M’Hamed, Morocco 2005 authors, unpub. data Sidi Ali Aguelmane, Morocco 2006 Fahd et al., 2007 Khandak Lanasser, Morocco 1992 Fahd and Pleguezuelos, 2001 Jbel Tidghine, Morocco 2005 Fahd et al., 2006 Ain Zora, Morocco 1992 Fahd and Pleguezuelos, 2001 Ras El Ma, Morocco 1908 Collection MNCN Madrid Moulouya river mouth, Morocco 1988 Collection Univ. Salamanca Saïdia, Morocco 1958 Bons, 1958 Aïn Benian, Algeria 1891 Collection MNHN Paris Djebel Heidzer, Algeria 2005 authors, unpub. data Tikjda, Algeria 2004 authors, unpub. data Darna, Algeria 2004 authors, unpub. data Darna, Algeria 2005 authors, unpub. data Ait Ouabane, Algeria 2005 authors, unpub. data Akfadou, Algeria 2006 authors, unpub. data Mountain Edough, Algeria 1977 Saint-Girons, 1977 Annaba, Algeria 1901 Collection MNHN Paris Ain Soltane, Tunisia 1953 Chpakowsky and Chnéour, 1953 Ain Draham, Tunisia 1953 Chpakowsky and Chnéour, 1953 109Climate change and relict viper populations forced using four localities (Table 1) where vipers were observed outside the temporal range of pre- sent environmental data, 1950 to 2000 (Hijmans et al., 2005). Removing such localities would imply an even smaller sample size for calibrating models, which would probably increase uncertainties in model predictions. Ecological Niche-based models Models were developed with Maximum Entropy approach, using MaxEnt 3.3.0f (Phillips et al., 2006). This modelling technique requires only presence data as input, but consistently performed well in comparison to other methods, especially at low samples sizes and in assessments of climate change effects (Elith et al., 2006; Hernandez et al., 2006; Hijmans and Graham, 2006; Wisz et al., 2008). A total of 25 replicates were run with random seed, which allows a different random 20% test / 80% train data partition in each run. Presence data for each replicate were chosen by bootstrap allowing sampling with replacement. Models were run with auto-features (Phillips et al., 2006), and the Area under the Curve (AUC) of the receiver-operating characteristics (ROC) plot was taken as a measure of individual model fit (Liu et al., 2005). The importance of an EGV for explaining the species distribution was determined by its aver- age percent contribution to the model. The relationship between viper occurrence and EGVs was determined by examination of response curves profiles from univariate models (Martínez-Freiría et al., 2008; Brito et al., 2008, 2009). The individual model replicates (N = 25) were added to generate a mean forecast of prob- ability of species presence under present climatic conditions (Araújo and New, 2007; Marmion et al., 2009). Standard deviation between individual model probabilities of occurrence was used as an indi- cation of prediction uncertainty (Buisson et al., 2010; Carvalho et al., 2010). The individual mod- el replicates were projected for each GCM and emission scenario, resulting in 150 simulations for each year. Models were averaged by year to generate a future probability of presence. The maximum standard deviation between replicate uncertainties across combinations of GCMs and emission sce- narios were taken as a measure of final prediction uncertainty. The consensus predictions of mean models were reclassified into three categories of habi- tat suitability: core habitats with more than 0.5 mean probability of occurrence, marginal habi- tats (between 0.25 and 0.5) and unsuitable habitats (less than 0.25). The area of each category was quantified and percentage change of each category from the present to the future predicted models were calculated (Carvalho et al., 2010). Total presence data (N = 33) were overlaid with present and future mean models to calculate percentages of presences in each habitat suitability category. Table 2. Environmental variation (minimum - maximum) in the study area in the present time and pre- dicted for 2020, 2050, 2080 from the ensemble of two emission scenarios (A2a and B2a) and three global circulation models (CCCMA, CSIRO and HADCM3). Variable Units Current 2020 2050 2080 ANPR mm 168 - 1430 156 - 1423 152 - 1370 131 - 1276 TANR ºC 18.4 - 36.9 18.3 - 38.6 17.8 - 39.7 18.2 - 40.9 TMAX ºC 25.7 - 37.2 26.4 - 40.7 27.6 - 40.8 28.8 - 43.7 ANTE ºC 4.2 - 20.1 5.3 - 21.4 6.6 - 22.3 7.3 - 24.6 SLOP % 0 - 69 - - - 110 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos RESULTS The ROC plots for the training and testing datasets exhibited high average AUCs (above 0.934 and 0.886, respectively) with low standard deviations (Table 3). All observations in the present model were identified as occurring in core and marginal habitat suitability areas. Annual average precipitation was the EGV most related to occurrence (average contri- bution above 58%), but slope (above 13%), annual temperature range (above 9%), and maxi- Table 3. Sample sizes, average (and standard deviation) training and test AUC, and average percent (and standard deviation) contribution of each variable for the 25 Maximum Entropy models projected to four climatic scenarios (Present, 2020, 2050 and 2080), and number (and percentage) of observations of Vipera latastei in North-western Africa in each habitat suitability category in each climatic scenario. Present 2020 2050 2080 N training samples 26 per model 26 per model 26 per model 26 per model N test samples 7 per model 7 per model 7 per model 7 per model Training AUC (SD) 0.935 (0.013) 0.934 (0.018) 0.934 (0.019) 0.935 (0.018) Test AUC (SD) 0.895 (0.067) 0.886 (0.093) 0.887 (0.087) 0.892 (0.087) ANPR (SD) 57.7 (14.1) 64.7 (15.6) 63.7 (15.2) 63.0 (17.2) TANR (SD) 9.0 (5.4) 11.0 (9.4) 9.3 (6.6) 9.8 (8.3) TMAX (SD) 9.1 (9.4) 7.9 (8.8) 9.4 (11.9) 8.2 (11.7) ANTE (SD) 6.4 (6.7) 3.6 (5.8) 4.0 (5.1) 3.6 (4.7) SLOP (SD) 17.7 (11.2) 12.8 (9.3) 13.6 (13.4) 15.5 (11.7) Suitability category Unsuitable (%) 0 (0) 3 (9.1) 6 (18.2) 8 (24.2) Marginal (%) 16 (48.5) 14 (42.4) 17 (51.5) 22 (66.7) Core (%) 17 (51.5) 16 (48.5) 10 (30.3) 3 (9.1) Fig. 2. Response curves for the most related environmental factors to the distribution of Vipera latastei in North-western Africa. Curves depict probability of occurrence along the environmental gradients. 111Climate change and relict viper populations Fig. 3. Mean probability of occurrence of Vipera latastei in North-western Africa, at a 1x1km scale, for the present and projected models (2020, 2050 and 2080), based on three global circulation models (GCM) and two emission scenarios (150 bootstrap models for each year). Maximum standard deviation of predic- tions across GCMs and scenarios are represented in smaller insets. 112 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos mum temperature of warmest month (above 8%) were also related (Table 3). The profiles of the response curves suggest that the species is restricted to precipitation and slopes roughly above 900 mm and 15%, respectively, and maximum temperatures below 30 ºC (Fig. 2). Core habitat-suitability areas according to the present model (Fig. 3) were fragment- ed and restricted to the Rif and few cells in central Middle Atlas and coastal Tangier in Morocco, eastern Tellian Atlas in Algeria, and El Feidja in Tunisia. Marginal suitability habitats surrounded core areas and included also the Middle Atlas and coastal regions of Salé, Melilla, Saidia and Oran. The areas of prediction uncertainty were common to the habitats identified as marginal and core. Future projection of models predicted a progressive decrease in the availability of suit- able areas (Table 4). Compared with the model for the present time, a decrease of 89% and 57% in the availability of core and marginal habitats, respectively, is predicted by 2080. Core habitat areas will be extremely fragmented and restricted to the Rif and Tellian mountains (Fig. 3) and would include only 9% of present-day viper localities in core areas (Table 3). The distribution of future predicted suitability areas suggests that most current- viper localities (67%) will be located in marginal habitats (Table 4). Areas of prediction uncertainty were restricted to few squares, especially for 2080 (Fig. 3). DISCUSSION The low number of observations available, the large dimensions of the study area and the projection to future climates stressed the importance of incorporating distinct sources of uncertainty in model projections for future climatic conditions. First, average predic- tions from different GCMs and emission scenarios were analysed, which allowed recover- ing patterns emerging from the noise associated with distinct model outputs (Buisson et al., 2010; Carvalho et al., 2010). Secondly, average predictions from model replicates using distinct presence data sets were analysed, which partially accounted for the effects of low sample size (Pearson et al., 2007). The Maximum Entropy algorithm was employed due to its good performance under climate change scenarios (Hijmans and Graham, 2006) and ability to deal with low sample sized data sets (Elith et al., 2006; Hernandez et al., 2006; Wisz et al., 2008). However, uncertainties associated to modelling techniques have been emphasised (Thuiller, 2004; Wiens et al., 2009; Buisson et al., 2010) and should be Table 4. Forecasted evolution of habitat suitability for Vipera latastei in North-western Africa. Number of 1x1 km squares classified by the present model and 2020, 2050 and 2080 scenarios in each habitat suit- ability category (unsuitable, marginal and core habitat). Percentage of gain (+) or loss (-) in number of squares relatively to the present model are given in brackets. Unsuitable Marginal Core Present 103958 47905 7609 2020 120751 (+16.2) 32493 (-32.2) 6228 (-18.1) 2050 131074 (+26.1) 25120 (-47.6) 3278 (-56.9) 2080 142193 (+36.8) 16440 (-65.7) 839 (-89.0) 113Climate change and relict viper populations addressed in future studies. Nevertheless, models were apparently robust and all presence data were identified in core and marginal areas of present model predictions. Uncertain- ties in projections of models related to low sample size were mostly located in cells identi- fied with core and marginal suitability, but not in cells of unsuitable habitat, suggesting that potential areas for the occurrence of the viper may actually be smaller, on average, than predicted. Present models were calibrated with restricted-range of environmen- tal conditions in comparison to the predicted environmental range for the future (Table 2) which may produce biases in model projections for the future (Barbet-Massin et al., 2010). However, the lower precipitation and higher temperatures predicted for the future that fall outside the present variation, mostly located in lower altitude areas between the Rif and Middle Atlas of Morocco and south-eastern valleys of El Feidja in Tunisia (data not shown), correspond already to present-day unsuitable areas (Fig. 3). The uncertain- ties arriving from these biases are thus negligible because these areas are very unlikely to become suitable habitats in the future. About 65% of the study area was quantified as unsuitable in the present model, which agrees with the biogeographical pattern of the peripheral limit of a species distribution. The proximity of the Sahara desert as a true ecological barrier for V. latastei further sup- ports the observed relationship between high annual precipitation and low maximum temperature with species presence. Presently, V. latastei is less common in flatter areas, which correspond essentially to coastal and agricultural regions, and slope is probably acting as surrogate for habitat loss in plain areas where human activities tend to be more intense (Charco, 1999; Ramdani et al., 2001; Cuttelod et al., 2008). In fact, local extinction in Morocco was suggested for coastal regions, where recent intensive sampling effort (Fahd and Pleguezuelos, 2001; Fahd et al., 2005, 2007; Harris et al., 2008; authors, unpub. data) failed to confirm previ- ous observations. These localities corresponded to coastal cells located in the Salé beach, Moulouya mouth and Tangiers peninsula, and have been most affected recently by tour- ism urbanisation (Ramdani et al., 2001; Fahd et al., 2005) that probably induced severe habitat loss for the viper. Local extinction in the coastal belt is a pattern also reported for the snake community of Mediterranean coastal Spain, deriving from intense tourism and agricultural activities (Santos et al., 2006, 2007b). The modelling approach used in this study considered all observations available because the secretive behaviour of the viper hampers the accurate determination of local extinction. However, if the suggested disap- pearance from certain areas of coastal Morocco is confirmed, then the current predictions of suitable habitats may be overestimated, as well as future range predictions. Present suitable areas for V. latastei in North-western Africa are fragmented and most- ly restricted to mountain areas of low habitat change. Most recent observations come from protected areas holding forests of high environmental and economic value, where grazing is relatively restricted to favour natural seedling. Alarmingly, pine plantations (e.g., in North- western Tunisia, Brito et al., 2008), cannabis culture (in the Rif, Fahd et al., 2005), and extensive agriculture and overexploitation of livestock outside protected areas, continue to threaten habitats (Charco, 1999). The models further suggested that the species may be pre- sent in currently undetected mountains, such as in Jbel Bou Naceur (Morocco). Likewise, large core habitat areas in Algeria were predicted for eastern Tellian Atlas, but field work is needed to confirm viper presence in these politically unstable areas. 114 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos Future projections are not optimistic for viper persistence, given the predicted declines in suitable habitats with no new suitable areas identified. The significant increase of temperature in North Africa during the mid-Piacenzian warm interval (ca 3 Myr ago) of the Late Pliocene (Jost et al., 2009) probably induced refugia in suitable mountain val- leys during warming stages and triggered for the current fragmented range of V. latastei. Thus, the projected decrease in precipitation (Paeth and Thamm, 2007) should imply even smaller suitable areas in the future. Dispersal was suggested as a possible mechanism for decreasing the impacts of climate change (e.g., Araújo et al., 2006), but severe popula- tion declines are expected in species with low dispersal capacities surrounded already by unsuitable habitats (Foden et al., 2007). In the case of V. latastei, colonisation of new cells is highly unlikely during the time-period of the study, given its climatic specialisation in North Africa and the systematically occurrence in preserved habitats (Real et al., 1997; Fahd and Pleguezuelos, 2001). This pattern is consistent with the Iberian Peninsula, where this viper is present in various habitat types (from coastal dunes to highland shrublands) but preferably in localities where habitats are well preserved (Santos et al., 2006). Addi- tionally, several biological traits of this viper make it a slow coloniser (Brito and Rebelo, 2003; Pleguezuelos et al., 2007; Santos et al., 2007b). According to future predictions, mountains will become climatic refugia, as predicted also for Cedrus atlantica forests in Morocco (Cheddadi et al., 2009). Therefore, the cur- rently existing mountain parks are priority areas for the conservation of this species. Although it is unknown if species will be able to adapt to future climate conditions and persist in the current range, monitoring of population trends and full protection of moun- tain forests are key-targets for long-term conservation of V. latastei in North Africa. How- ever, current predictions should also be evaluated for the first projected scenario (year 2020), with viper sampling in current suitable habitats and/or confirmation of forecast- ed decrease in precipitation. Field sampling should take into account detectability bias- es related to rareness and cryptic behaviour (Mazerolle et al., 2007). If predicted reduc- tions in habitat suitability to 2020 are correct, conservation actions must be accomplished, including the strict protection of all areas with viper populations, the exclusion of grazing from these areas, and potentially population translocation. Under the scenario of habitat suitability decrease in 2020, the delay of these management actions would be catastrophic for long-term conservation of this viper. Trends in the availability of suitable habitats observed in this study may give indica- tions about other European-originated vertebrates with relict populations in North Africa, including fishes (Barbus sp.), amphibians (Salamandra algira), reptiles (Coronella girondi- ca), birds (Cinclus cinclus), and mammals (Mustela putorius), which should evidence simi- lar environmental responses and extinction risks as the studied viper. The conservation of these species would benefit from modelling procedures to examine their distribution tendencies which would assist in management actions for their conservation. ACKNOWLEDGEMENTS This study was partially supported by project POCTI/BIA-BDE/55596/2004 from Fundação para a Ciência e Tecnologia (FCT, Portugal) and by Cooperation CNRST-FCT (2008-09). JCB has a 115Climate change and relict viper populations contract (Programme Ciência 2007). FMF and PT have grants (SFRH/BPD/69857/2010 and SFRH/ BD/42480/2007, respectively) from FCT. Acknowledgments extended to the numerous researchers who gave unpublished observations. REFERENCES Araújo, M.B., New M. (2007): Ensemble forecasting of species distributions. TREE 22: 42-47. Araújo, M.B., Thuiller, W., Pearson, R.G. (2006): Climate warming and the decline of amphibians and reptiles in Europe. J. Biogeogr. 33: 1712-1718. Barbet-Massin, M., Thuiller, W., Jiguet, F. (2010): How much do we overestimate future local extinction rates when restricting the range of occurrence data in climate suit- ability models? Ecography 33: 878-886. Boettger, O. (1883): Die Reptilien und Amphibien von Marokko II. Abhandl. Senckenb. Ges. 13: 93-146. Bons, J. (1958): Contribution a l’étude de l’herpétofaune marocaine (Reptiles de la région d’Ifrane). Bull. Soc. Sci. Nat. Phys. Maroc 38: 167-182. Bons, J. (1963): Notules herpétologiques marocaines. Comptes Rendus des Sèances Men- suelles de la Société des Sciences Naturelles et Physiques du Maroc 29: 135-137. Bons, J., Geniez, Ph. (1996). Amphibiens et Reptiles du Maroc. AHE, Barcelona. Brito, J.C., Acosta, A.L., Álvares, F., Cuzin, F. (2009): Biogeography and conservation of taxa from remote regions: An application of ecological-niche based models and GIS to North-African canids. Biol. Conserv. 142: 3020-3029. Brito, J.C., Rebelo, R. (2003): Differential growth and mortality affect sexual size dimor- phism in Vipera latastei. Copeia 2003: 865-871. Brito, J.C., Santos, X., Pleguezuelos, J.M., Sillero, N. (2008): Inferring evolutionary scenar- ios with geostatistics and geographical information systems for the viperid snakes Vipera latastei and Vipera monticola. Biol. J. Linn. Soc. 95: 790-806. Buisson, L., Thuiller, W., Casajus, N., Lek, S., Grenouillet, G. (2010): Uncertainty in ensemble forecasting of species distribution. Glob. Chang. Biol. 16: 1145-1157. Carvalho, S.B., Brito, J.C., Crespo, E.J., Possingham, H.P. (2010): From climate change pre- dictions to actions – conserving vulnerable animal groups in hotspots at a regional scale. Glob. Chang. Biol. 16: 3257–3270. Charco, J. (1999): El Bosque Mediterráneo en el Norte de África: biodiversidad y lucha contra la desertificación. Agencia Española de Cooperación Internacional, Madrid. Cheddadi, R., Fady, B., François, L., Hajar, L., Suc, J.-P., Huang, K., Demarteau, M., Ven- dramin, G.G., Ortu, E. (2009): Putative glacial refugia of Cedrus atlantica deduced from Quaternary pollen records and modern genetic diversity. J. Biogeogr. 36: 1361-1371. Chpakowsky, N., Chnéour, A. (1953): Les serpents de Tunisie. Bull. Soc. Sci. Nat. Tunisie 6: 125-146. Cuttelod, A., García, N., Abdul Malak, D., Temple, H., Katariya, V. (2008): The Mediter- ranean: a biodiversity hotspot under threat. In: The 2008 Review of the IUCN Red List of Threatened Species. Vié, J.C., Hilton-Taylor, C., Stuart, S.N., Eds, IUCN, Gland. 116 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos Czech, B., Krausman, P.R. (1997): Distribution and causation of species endangerment in the United States. Science 277: 1116-1117. De Jong, H. (1998): In search of historical biogeographic patterns in the western Mediter- ranean terrestrial fauna. Biol. J. Linn. Soc. 65: 99-164. Dolfus, R.P., Beaurieux, C. (1928): Tableau pour la détermination facile des serpents du Maroc. Var. Sci. Soc. Sci. Nat. Phys. Maroc 1: 1-29. Elith, J., Graham, C.H., Anderson, R.P., Dudyk, M., Freer, S., Guisan, A., Hijmans, R.J., Huettmann, F., Leathwick, J.R., Lehmann, A., Li, J., Lohmann, L.G., Loiselle, B.A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., McOverton, J., Peterson, A.T., Phillips, S., Wisz, M.S., Zimmermann, N.E. (2006): Novel methods improve predic- tion of species’ distributions from occurrence data. Ecography 29: 129-151. Fahd, S., Barata, M., Benítez, M., Brito, J.C., Caro, J., Carvalho, S., Chirosa, M., Feriche, M., Herrera, T., Márquez-Ferrando, R., Nesbitt, D., Pleguezuelos, J.M., Reques, R., Paz Rodríguez, M., Santos, X., Sicilia, M., Vasconcelos, R. (2007): Presencia de la víbora hocicuda Vipera latastei en el Atlas Medio (Marruecos) y otras citas herpe- tológicas para la región. Bol. Asoc. Herpetol. Esp. 18: 26-34. Fahd, S., Benítez, M., Brito, J.C., Caro, J., Chirosa, M., Feriche, M., Fernández-Cardenete, J.R., Martínez-Freira, F., Márquez-Ferrando, R., Nesbitt, D., Pleguezuelos, J.M., Reques, R., Paz Rodríguez, M., Santos, X., Sicilia, M. (2005): Distribución de Vipera latastei en el Rif y otras citas herpetológicas para el norte de Marruecos. Bol. Asoc. Herpetol. Esp. 16: 19-25. Fahd, S., Pleguezuelos, J.M. (2001): Los reptiles del Rif (Norte de Marruecos), II: anfis- benios y ofidios. Comentarios sobre la biogeografia del grupo. Rev. Esp. Herpetol. 15: 13-36. Foden, W., Midgley, G.F., Hughes, G., Bond, W.J., Thuiller, W., Hoffman, M.T., Kaleme, P., Underhill, L.G., Rebelo, A., Hannah, L. (2007): A changing climate is eroding the geographical range of the Namib Desert tree Aloe through population declines and dispersal lags. Divers. Distrib. 13: 645-653. Harris, D.J., Carretero, M.A., Brito J.C., Kaliontzopoulou, A., Pinho, C., Perera A., Vas- concelos R., Barata M., Barbosa, D., Carvalho, S., Fonseca, M.M., Pérez-Lanuza, G., Rato, C. (2008): Data on the distribution of the terrestrial herpetofauna of Morocco: records from 2001-2006. Herpetol. Bull. 103: 19-28. Hernandez, P.A., Graham, C.H., Master, L.L., Albert, D.L. (2006): The effect of sample size and species characteristics on performance of different species distribution mode- ling methods. Ecography 29: 773-785. Hewitt, G.M. (2000): The genetic legacy of the Quaternary ice ages. Nature 405: 907-913. Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A. (2005): Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25: 1965-1978. Hijmans, R.J., Graham, C.H. (2006): The ability of climate envelope models to predict the effect of climate change on species distributions. Glob. Chang. Biol. 12: 2272-2281. IPCC-TGICA (2007): General Guidelines on the Use of Scenario Data for Climate Impact and Adaptation Assessment. Version 2. Prepared by T.R. Carter on behalf of the IPCC, Task Group on Data and Scenario Support for Impact and Climate Assessment. Jost, A., Fauquette, S., Kageyama, M., Krinner, G., Ramstein, G., Suc, J.-P., Viollete, S. (2009): High resolution climate and vegetation simulations of the Late Pliocene, a 117Climate change and relict viper populations model-data comparison over Western Europe and the Mediterranean region. Cli- mate in the Past 5: 585-606. Liu, C., Berry, P.M., Dawson, T.P., Pearson, R.G. (2005): Selecting thresholds of occurrence in the prediction of species distributions. Ecography 28: 385-393. Marmion, M., Parviainen, M., Luoto, M., Heikkinen, R.K.., Thuiller, W. (2009): Evaluation of consensus methods in predictive species distribution modelling. Divers. Distrib. 15: 59-69. Martínez-Freiría, F., Sillero, N., Lizana, M., Brito, J.C. (2008): GIS-based niche mod- els identify environmental correlates sustaining a contact zone between European vipers. Divers. Distrib. 14: 452-461. Mazerolle, M.J., Bailey, L.L., Kendall, W.L., Royle, J.A., Converse, S.J., Nichols, J.D. (2007): Making great leaps forward: accounting for detectability in herpetological field stud- ies. J. Herpetol. 41: 672-689. Mediani, M., Amezian, M., Tattou, M.I., Benhoussa, A., Idrissi, H.R., El Agbani, M.A., Qninba, A. (2009): Nouvelles citations de deux espèces reliques paléarctiques, Emys orbicularis Linnaeus, 1758 et Vipera latastei Boscá, 1878 dans la Péninsule Tingitane (Rif occidental, Maroc). Bulletin de l’Institut Scientifique, Rabat 31: 99-102. Nogués-Bravo, D., Araújo, M.B., Errea, M.P., Martínez-Rica, J.P. (2007): Exposure of glob- al mountain systems to climate warming during the 21st Century. Glob. Environ. Change 17: 420-428. Paeth, H., Thamm, H.-H. (2007): Regional modelling of future African climate north of 15ºS including greenhouse warming and land degradation. Clim. Change 83: 401-427. Pearson, R.G., Raxworthy, C.J., Nakamura, M., Peterson, A.T. (2007): Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. J. Biogeogr. 34: 102-117. Peterson, A.T. (2003): Projected climate change on Rocky Mountain and Great plains birds: generalities of biodiversity consequences. Glob. Chang. Biol. 9: 647-655. Phillips, S.J., Anderson, R.P., Schapire, R.E. (2006): Maximum entropy modeling of species geographic distributions. Ecol. Modell. 190: 231-259. Pleguezuelos, J.M., Brito, J.C., Fahd, S., Feriche, M., Mateo, J.A., Moreno-Rueda, G., Reques, R., Santos, X. (2010). Setting conservation priorities for the Moroccan her- petofauna: the utility of Regional Red Listing. Oryx 44: 501–508. Pleguezuelos, J.M., Santos, X., Brito, J.C., Parellada, X., Llorente, G.A., Fahd, S. (2007): Reproductive ecology of Vipera latastei, in the Iberian Peninsula: Implications for the conservation of a Mediterranean viper. Zoology 110: 9-19. Ramdani, M., Flower, R.J., Elkhiati, N., Kraiem, M.M., Fathi, A.A., Birks, H.H., Patrick, S.T. (2001): North African wetland lakes: characterization of nine sites included in the CASSARINA project. Aquat. Ecol. 35: 281-302. Real, R., Pleguezuelos, J.M., Fahd, S. (1997): The distribution patterns of reptiles in the Rif region, northern Morocco. Afr. J. Ecol. 35: 312-325. Rodrigues, A.S.L., Gaston, K.J. (2002): Rarity and conservation planning across geopoliti- cal units. Cons. Biol. 16: 674-682. Saint-Girons, H. (1977): Systématique de Vipera latastei latastei Boscá, 1878 et descrip- tion de Vipera latastei gaditana, subsp. n. (Reptilia, Viperidae). Rev. Suisse Zool. 84: 599-607. 118 J.C. Brito, S. Fahd, F. Martínez-Freiría, P. Tarroso, S. Larbes, J.M. Pleguezuelos and X. Santos Saint-Girons, H. (1980): Biogéographie et évolution des vipéres européennes. C. R. Soc. Biogeogr. 496: 146-172. Samways, M.J. (2003): Marginality and national red listing of species. Biodiv. Cons. 12: 2523-2525. Santos, X., Brito, J.C., Caro, J., Abril, A.J., Lorenzo, M., Sillero, N., Pleguezuelos, J.M. (2009): Habitat suitability, threats and conservation of isolated populations of the smooth snake (Coronella austriaca) in the southern Iberian Peninsula. Biol. Con- serv. 142: 344-352. Santos, X., Brito, J.C., Pleguezuelos, J.M., Llorente, G.A. (2007b): Comparing Filippi and Luiselli’s (2000) method with a cartographic approach to assess the conservation sta- tus of secretive species: the case of the Iberian snake-fauna. Amphibia-Reptilia 28: 17-23. Santos, X., Brito, J.C., Sillero, N., Pleguezuelos, J.M., Llorente, G.A., Fahd, S., Parellada, X. (2006): Inferring habitat-suitability areas with ecological modelling techniques and GIS: A contribution to assess the conservation status of Vipera latastei. Biol. Con- serv. 130: 416-425. Santos, X., Llorente, G.A., Pleguezuelos, J.M., Brito, J.C., Fahd, S., Parellada, X. (2007a): Variation in the diet of the Lataste’s viper Vipera latastei in the Iberian Peninsula: seasonal, sexual and size-related effects. Animal Biol. 57: 49-61. Schleich, H.H., Kästle, W., Kabisch, K. (1996): Amphibians and Reptiles of North Africa. Koeltz Scientific Books, Koenigstein. Sindaco, R., Jeremcenko, V.K. (2008): The Reptiles of the Western Palearctic 1. Edizioni Belvedere, Latina. Thuiller, W. (2004): Patterns and uncertainties of species’ range shifts under climate change. Glob. Chang. Biol. 10: 2020-2027. USGS (2006): Shuttle Radar Topography Mission (SRTM). USGS. http://srtm.usgs.gov/ index.html. Wiens, J.A., Stralberg, D., Jongsomjit, D., Howell, C.A., Snyder, M.A. (2009): Niches, mod- els, and climate change: assessing the assumptions and uncertainties. PNAS 106: 19729-19736. Wisz, M.S., Hijmans, R.J., Li, J., Peterson, A.T., Graham, C.H., Guisan, A., NCEAS Pre- dicting Species Distribution Working Group (2008): effects of sample size on the performance of species distribution models. Diversity and Distributions 14: 763-773. bbib67 OLE_LINK1 OLE_LINK2 bbib28 OLE_LINK5 OLE_LINK6 OLE_LINK7 OLE_LINK8 _GoBack OLE_LINK1 OLE_LINK2 OLE_LINK3 OLE_LINK4 OLE_LINK1 OLE_LINK2 OLE_LINK19 OLE_LINK20 OLE_LINK21 OLE_LINK29 OLE_LINK3 OLE_LINK4 OLE_LINK5 OLE_LINK31 OLE_LINK14 OLE_LINK15 OLE_LINK12 OLE_LINK13 OLE_LINK16 OLE_LINK17 OLE_LINK22 OLE_LINK23 OLE_LINK24 OLE_LINK8 OLE_LINK9 OLE_LINK10 OLE_LINK11 OLE_LINK18 OLE_LINK27 OLE_LINK28 OLE_LINK25 OLE_LINK26 OLE_LINK6 OLE_LINK7 OLE_LINK34 OLE_LINK37 OLE_LINK38 Acta Herpetologica Vol. 6, n. 1 - June 2011 Firenze University Press Widespread bacterial infection affecting Rana temporaria tadpoles in mountain areas Rocco Tiberti Extreme feeding behaviours in the Italian wall lizard, Podarcis siculus Massimo Capula1, Gaetano Aloise2 Lissotriton vulgaris paedomorphs in south-western Romania: a consequence of a human modified habitat? Severus D. Covaciu-Marcov*, Istvan Sas, Alfred Ş. Cicort-Lucaciu, Horia V. Bogdan Body size and reproductive characteristics of paedomorphic and metamorphic individuals of the northern banded newt (Ommatotriton ophryticus) Eyup Başkale1, Ferah Sayım2 , Uğur Kaya2 Genetic characterization of over hundred years old Caretta caretta specimens from Italian and Maltese museums Luisa Garofalo1, John J. Borg2, Rossella Carlini3, Luca Mizzan4, Nicola Novarini4, Giovanni Scillitani5, Andrea Novelletto1 The phylogenetic position of Lygodactylus angularis and the utility of using the 16S rDNA gene for delimiting species in Lygodactylus (Squamata, Gekkonidae) Riccardo Castiglia*, Flavia Annesi Localization of glucagon and insulin cells and its variation with respect to physiological events in Eutropis carinata Vidya. R. Chandavar1, Prakash. R. Naik2* The Balearic herpetofauna: a species update and a review on the evidence Samuel Pinya1, Miguel A. Carretero2 Effects of mosquitofish (Gambusia affinis) cues on wood frog (Lithobates sylvaticus) tadpole activity Katherine F. Buttermore, Paige N. Litkenhaus, Danielle C. Torpey, Geoffrey R. Smith*, Jessica E. Rettig Food composition of Uludağ frog, Rana macrocnemis Boulenger, 1885 in Uludağ (Bursa, Turkey) Kerim Çiçek Preliminary results on tail energetics in the Moorish gecko, Tarentola mauritanica Tommaso Cencetti1,2, Piera Poli3, Marcello Mele3, Marco A.L. Zuffi1 Climate change and peripheral populations: predictions for a relict Mediterranean viper José C. Brito1, Soumia Fahd 2, Fernando Martínez-Freiría1, Pedro Tarroso1, Said Larbes3, Juan M. Pleguezuelos4, Xavier Santos5 Assessing the status of amphibian breeding sites in Italy: a national survey Societas Herpetologica Italica* Osservatorio Erpetologico Italiano ACTA HERPETOLOGICA Journal of the Societas Herpetologica Italica ACTA HERPETOLOGICA Rivista della Societas Herpetologica Italica