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Biological Conservation 142 (2009) 3020–3029
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Biological Conservation
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Biogeography and conservation of taxa from remote regions: An application of ecological-niche based models and GIS to North-African Canids
José C. Brito a,*, André L. Acosta a, Francisco Álvares a, Fabrice Cuzin b a CIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos da Universidade do Porto, Instituto de Ciências Agrárias de Vairão, R. Padre Armando Quintas, 4485-661 Vairão, Portugal b BP 1172 Bab Agnaw, 40.000 Marrakech, Morocco article info abstract
Article history: In North Africa, and especially in the Sahara Desert, biodiversity is poorly known. Of the five widespread Received 4 March 2009 canid species present, one is Data Deficient, three are considered widespread although habitat selection Received in revised form 30 July 2009 could limit their area of occupancy, and distribution maps available are coarse for conservation planning. Accepted 3 August 2009 This study identifies biogeographic patterns in North-African Canids through the combination of high res- Available online 11 September 2009 olution presence data with 16 environmental factors. Predictive models trained in north-west Africa are projected to all North Africa. Canids exhibited distinct biogeographical affinities. GIS tools and Maximum Keywords: Entropy models identify a mixture of climatic and habitat factors as main predictors of species occur- Canis rence. Suitable habitats for North-African Canids are mostly fragmented: probable occurrence was iden- Maxent Predicted distribution tified for Canis aureus in Saharan peripheral regions and mountains, for Vulpes pallida in a narrow band Sahara desert along the Sahel and in southern Saharan mountains, for Vulpes rueppellii throughout the Sahara, for Vulpes Sympatry vulpes in northern Africa until the Sahara northern limit, and for Vulpes zerda in almost all Sahara. Areas of Vulpes potential sympatry between species with similar niches and parapatric ranges are identified along rela- tively narrow bands. The small pixel size of projections allows the identification of suitable refuges for species otherwise absent in the driest Saharan habitats, providing framework data for the definition of the global conservation status of V. pallida, and conservation strategies for the guild. The biological value of Saharan mountains is emphasised as they constitute isolated suitable areas. Ecological-niche based models should be developed for other endangered Saharan vertebrates. Ó 2009 Elsevier Ltd. All rights reserved.
1. Introduction or elusive behaviour (Álvares and Brito, 2006; Torres et al., 2009). Thus, many species occurring in remote regions are poorly Biodiversity faces currently an unprecedented crisis resulting known, concerning the extent of occurrence, area of occupancy from increasing levels of species extinction and habitat fragmenta- and population trends, being usually classified has Data Deficient tion. The identification of biodiversity hotspots, areas with simul- (DD) according to the Red List criteria (IUCN, 2001). taneously high biodiversity and extinction risk, and the Compared with non-Saharan Northern Africa where data are characterization of a set of paradigmatic rules to systematic con- more abundant, the Sahara Desert is a remarkable example of a re- servation planning are first steps to halt biodiversity loss (Myers gion where biodiversity is poorly known as a consequence of its et al., 2000; Margules and Pressey, 2000). But how can we imple- remoteness and frequent civil unrest (Archer and Popovic, 2007; ment biodiversity management if in many cases the distribution Ward, 2009). With about 8,000,000 km2, the Sahara is the largest of biodiversity itself is vaguely known? Many hotspots are located desert in the world which renders logistic difficulties for sampling. in regions difficult to sample because of their remoteness and, fre- Regional conflicts hamper or even deny the scientific exploration of quently, civil unrest and war (Strange et al., 2008). Inaccessibility several key-areas, like isolated mountains that hold endemic plants produces lack of knowledge about distribution, hampering the and vertebrates (Quézel, 1978; Le Berre, 1989, 1990; Trape, 2009). accurate estimation of species conservation status. The collection As a result, much of the knowledge on Saharan biodiversity comes of key biological data necessary for identifying extinction-prone from historical exploratory missions and sporadic expeditions (e.g. taxa may be further harder in species with low population size Rebelo and Brito, 2007). These constraints commonly translate into coarse distribution maps, where the range is represented by con- tinuous polygons (Le Berre, 1989, 1990). These maps are useful * Corresponding author. Tel.: +351 252660411. for estimating the extent of occurrence of species, i.e. the area E-mail addresses: [email protected] (J.C. Brito), [email protected] (A.L. Acosta), [email protected] (F. Álvares), [email protected] (F. Cuzin). contained within the shortest continuous imaginary boundary
0006-3207/$ - see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2009.08.001 Author's personal copy
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(minimum convex polygon) which can be drawn to encompass all ment of conservation status of poorly known species (Papes and the present occurrences of a taxon (IUCN, 2001). Nevertheless, they Gaubert, 2007), and the design of reserves (Brito et al., 1999). are overestimations of the true area of occupancy, i.e. the area The aims of this study are to identify: (1) biogeographic pat- occupied (e.g. sum of the occupied grid squares) by a taxon within terns in species range; (2) environmental factors related to species its extent of occurrence (IUCN, 2001), since they do not take into occurrence; (3) probable areas for species occurrence; and (4) account particular unsuitable habitats where species may be ab- probable areas of sympatry among species with similar ecological sent. However, species presence data collected with high accuracy niches and parapatric ranges (V. vulpes, V. pallida and V. rueppellii). are crucial for the development of optimised conservation High resolution presence data (2 Â 2 km) collected in a training strategies. area (from Morocco to northern Senegal) will be combined with Five North-African canids illustrate well the lack of knowledge environmental factors to derive predictive models of species occur- on Saharan biodiversity: (1) the golden jackal, Canis aureus Lin- rence, which will be extrapolated to a projection area (all North naeus, 1758, is the largest and is widespread in North Africa, but Africa). Results of this study are intended to decrease the current habitat selection patterns are unknown resulting in probable over- lack of knowledge about distribution and occupied habitats by estimation of the true area of occupancy, and population decline is North-African canids, contributing for the future determination occurring except in protected areas (Sillero-Zubiri et al., 2004; Sil- of the conservation status of V. pallida. It is expected to provide a lero-Zubiri, 2009); (2) the pale fox, Vulpes pallida (Cretzschmar, methodological approach for the quantification of area of occu- 1827) is endemic to the semi-arid Sahelian region of Africa border- pancy for other highly endangered and/or ecologically similar ing the southern limit of the Sahara, from the Atlantic to the Red mammals in one of the most remote and barely studied regions Sea, and it is considered one of the least known canid species being of the world. classified as Data Deficient (DD); (3) the Rüppell’s fox, Vulpes rue- ppellii (Schinz, 1825) is known from desertic and semi-desertic re- 2. Materials and methods gions from the Atlantic coast to Somalia, but the status and ecology of North African populations remains largely unknown; (4) the red 2.1. Study areas and species observations fox, Vulpes vulpes Linnaeus, 1758, despite having the widest geo- graphical range of any member of the order Carnivora is restricted, Models were trained in north-west Africa (latitude from N14.6 in Africa, to the region north of the Sahara from where it might be to N35.9 and longitude from W1.0 to W17.5) in an area comprising expanding at the cost of V. rueppellii (Cuzin, 2003; Sillero-Zubiri Morocco, Western Sahara, Mauritania and northern Senegal, and et al., 2004); and (5) the fennec fox, Vulpes zerda (Zimmermann, projected to all of Africa north of N12.4 (Fig. 1). 1780), is the smallest and is widespread in sandy deserts and One additional canid is present in the training area, the side- semi-deserts but habitat selection patterns are unknown and local striped jackal (C. adustus), but it was not considered in this study population decline was documented in northern Moroccan Sahara since it presents peripheral populations (Sillero-Zubiri, 2009). (Cuzin, 2003). Overall, the most recent distribution maps for these canids are coarse and unsuitable for local scale systematic conser- vation planning (Sillero-Zubiri et al., 2004; Sillero-Zubiri, 2009). 2.1.1. Dataset for model training These canids form a guild since they have similar body sizes and A total of 627 observations of canids were used to develop mod- weights (Osborn and Helmy, 1980), exploit similar trophic niches, els for the training area, of which 291 were unpublished observa- being carnivores with accessory frugivory (Sillero-Zubiri et al., tions by the authors, 261 were unpublished observations given 2004), and partially compete (Yom-Tov and Mendelssohn, 1988; by other researchers and 75 observations came from bibliographic Cuzin, 2003). Given their wide range, they are likely to be charac- references (Appendix S2) and museum collections (Smithsonian teristic of all North African ecosystems. Three morphologically- Institute). Observations were collected from the period between similar species occur in distinct biogeographic regions, Sahelian 1932 and 2007, although 75% were from after 1990. Canid records in V. pallida, Saharo-Sindian in V. rueppellii and Mediterranean in were largely collected ad hoc with the exception of: (1) the Moroc- V. vulpes (Sillero-Zubiri, 2009), resulting in broadly parapatric can low Drâa river valley which was sampled more intensively for ranges, i.e. contiguous distributions with slight overlap. These spe- local studies on distribution of large mammals (Cuzin, 2003) and cies compete in contact zones and spatial exclusion may be driven (2) the Mauritanian inland regions of Tiris Zemmour and Majâbat by environmental and human-related factors. For instance, V. rue- al-Koubrâ which were not sampled due to their extreme ppellii is suspected to have suffered historical expansion of distri- remoteness. bution area related to desertification but limited by competition From the total number of observations, 397 were direct obser- with V. vulpes due to new human settlements (Cuzin, 2003; Sille- vations including live animals and dead specimens (mainly road ro-Zubiri et al., 2004). Therefore, the North African guild of wide- killed) and 230 were indirect observations including tracks, faeces, spread canids presents dynamic range scenarios related to vocalisations and inquiries to local shepherds. climate fluctuations and human activities which remain unex- Thirty-four tissue samples of road-killed specimens collected by plored (but see Cuzin, 2003). Furthermore, they probably provide authors were subjected to genetic identification due to uncertainty a taxonomically homogenous surrogate for other non-canid carni- in taxonomical diagnosis. A fragment of 360 bp of the mitochon- vores in the region, since they share many distinct habitats and are drial DNA cytochrome b gene was PCR-amplified using CB3-H subjected to common extinction risks. and the forward version of CB2-H primers (Palumbi, 1996) and se- The combination of ecological-niche based models with Geo- quenced both strands following the ABI PrismBigBye Terminator graphical Information Systems (GIS) has prompted conservation- Cycle sequencing protocol in an ABI 3100xl genetic analyser. Each biology studies with more robust analytical methods (Guisan and sample was unambiguously allocated to one species based on its Zimmermann, 2000). GIS are useful tools to analyse geographic-re- mtDNA haplotype. lated processes for conservation planning, such as the identifica- For 236 observations, the geographic location was recorded tion of suitable habitat areas for rare species (Gaubert et al., with a Global Positioning System (GPS) on the WGS84 datum, 2006) or over large and remote study areas (Travaini et al., whereas the remaining 391 observations were georeferenced using 2007), the estimation of population size for peripheral populations military maps (Institut Geographique National of France) to a pre- (Álvares and Brito, 2006; Santos et al., 2009), the prediction of cli- cision of less than 2.5 km. Many other observations were available mate-change induced range shifts (Thuiller et al., 2006), the assess- but were not used due to coarse georeferencing (e.g. 50 Â 50 km; Author's personal copy
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Fig. 1. Location of the training and projection areas within the African context and toponomies used in text.
Aulagnier and Thévenot, 1986). The 627 observations were subdi- ArcMap GIS, and distance grids were reclassified into distance clas- vided into two datasets (Appendix S3): one dataset with 377 obser- ses (Table 1). Class limits were set according to the average home- vations for training the models and another dataset with 250 range size of each canid: from <2.3 km of V. zerda up to >18.4 km of observations for testing the models. Criteria for selecting observa- C. aureus (Sillero-Zubiri, 2009). Finally, the resolution of all EGVs tions for the test dataset included: all observations prior to 1950, was decreased to a grid cell size of 0.025 decimal degrees observations consisting of tracks and faeces, all observations prior (2340 Â 2340 m) in the training area and to 0.106 decimal degrees to 1990 recorded in areas were major habitat changes occurred (9961 Â 9961 m) in the projection area. during the 20th century (western and north-western coastal Mor- occo), and whenever clusters of species occurrence were detected 2.3. Biogeographic patterns (mostly in the over-sampled low Drâa river valley). These criteria were intended to minimize uncertainties in current species pres- A Principal Components Analysis of one topographical and five ence, provide indications on the reliability of dubious records, climatic variables (Table 1; Hijmans et al., 2005) performed with and to decrease the level of spatial autocorrelation in species pres- the ‘‘Principal Components Analysis” extension of the GIS ArcMap ences. The ‘‘Nearest Neighbour Index” of ArcMap GIS assessed the 9.2 (ESRI, 2006) depicted the topoclimatic variability of the train- degree of clustering of the data and ranged from 0.49 in C. aureus to ing area (Appendix S1). The three first axes (explaining 92.5% of 0.88 in V. pallida, indicating some degree of clustering for the for- the variance of the training area) were assembled and classified mer and dispersed distribution for the latter. with the function ‘‘Maximum Likelihood” of ArcMap GIS. The train- ing presences were intersected with the topoclimatic grid using 2.1.2. Dataset to evaluate model projection the ‘‘Intersect Point Tool” extension for ArcMap GIS (Beyer, Five hundred and sixty presences from outside the training area 2006). The percentage of presences of each species in each topocli- were used to test projections to all North Africa. These were 10 matic unit was taken as a measure of the biogeographic affinities of unpublished observations by the authors, five observations from each species (Sillero et al., 2009). Selection among topoclimatic Algeria (S. Larbes, unpub. data) and 544 observations from biblio- units was quantified from the percentages of presences using the graphic references (Appendix S2). Presences were georeferenced to Standardised Levin’s B measure of niche breadth: Bs = B À 1/ the 10 Â 10 km resolution since several bibliographic references n À 1, where B is the Levin’s indexP and n the total number of topo- with many important observations were not available at finer-de- climatic units. B is given by 1/ (p2), where p is the proportion of tailed scales (e.g. Kowalski and Rzebik-Kowalska, 1991). presences in topoclimatic unit j.
2.2. Environmental factors 2.4. Model training in North-Western Africa
Three sets of environmental factors or ecogeographical vari- Models were developed with the Maximum Entropy approach ables (hereafter EGV) were selected for the ecological models (Phillips et al., 2006; Phillips and Dudík, 2008). This modelling according to their meaning to the ecology and distribution of Afri- technique requires only presence data as input, but consistently can carnivores (Gaubert et al., 2006; Thuiller et al., 2006; Papes and performed well in comparison to other methods (Elith et al., Gaubert, 2007). These sets included one topographical grid (USGS, 2006), especially at low samples sizes (Hernandez et al., 2006), 2006) that was used to derive Slope, with the ‘‘Slope” function of and it has been used successfully in ecological-niche based model- ArcMap GIS; five climate grids (Hijmans et al., 2005) slightly corre- ling (e.g. Papes and Gaubert, 2007; Brito et al., 2008; Martínez-Fre- lated (r < 0.60), with the exception of ANPR and PWET (r = 0.85); iría et al., 2008; Torres et al., 2009). and a land cover grid from the years 1999–2000 (GLC, 2003). Presence data and EGVs were imported into Maxent 3.0.4 beta One binary grid was created for each habitat type that covered software (http://www.cs.princeton.edu/~schapire/maxent). Four more than 0.5% of the study area. The Euclidean distance to the model types were developed in the training area using distinct closest source was calculated for each pixel of each individual hab- EGV sources (Table 1) and datasets: (1) a Topoclimatic model itat grid (10 habitat types) using the ‘‘Euclidian Distance” tool of (TMs) using the topographical (slope) and the five climatic EGVs Author's personal copy
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Table 1 Environmental factors used for model the distribution of canids in the training area.
Type Variable Range and units Code Topographical Slope From 0% to above 31% SLOP Climatic Temperature annual range From 10.9 to 41.9 °C TANR Minimum temperature of coldest month From À14.1 to 17.2 °C TMIN Maximum temperature of warmest month From 22.5 to 48.9 °C TMAX Annual precipitation From 6 to 1169 mm ANPR Precipitation of wettest month From 2 to 263 mm PWET Habitat Distance to evergreen forest Five classes: <2.3; 2.3–4.6; 4.6–9.2; 9.2–18.4; >18.4 km DEGFO Distance to closed deciduous forest DCDFO Distance to shrubland DSHRU Distance to closed grassland DCLGR Distance to open grassland DOPGR Distance to sparse grassland DSPGR Distance to cropland DCROP Distance to sandy desert and dunes DSAND Distance to stony desert DSTON Distance to bare rock DBROC
with the test dataset defined by selective criteria; (2) a Habitat sen because ‘true’ absence data was not available (Brito et al., model (HMs) using the distances to the 10 land cover types and 2008). Models were reclassified with ‘‘Reclassify” function of Arc- the testing selective criteria; (3) a Topoclimatic model (TMr) using Map GIS and finally they were overlaid to produce an Ensemble topoclimatic EGVs and all observations randomly separated in 80% Threshold model (EM). EMs displayed three categories of probabil- for training and 20% for testing; and (4) a Habitat model (HMr) ity: areas of high presence probability identified simultaneously by using habitat EGVs and also all observations randomly separated. TM and HM (presence high), areas of high presence probability These models were developed to compare how selective criteria identified by only one model type (presence moderate), and areas performed relatively to the classical approach of random data split- identified with high absence probability by two model types (ab- ting into training and test sets. Models were run with auto-features sence). The percentage of the projection area identified with high (Phillips et al., 2006) and the Area under the Curve (AUC) of the presence probability was calculated from the reclassified TM and ROC plot was taken as a measure of the overall fit of the models HM models individually and from the EM. In the EM, potential (Liu et al., 2005). areas included areas identified with high probability at least by The importance of each EGV for explaining the distribution of one of the two individual models and by the two models simulta- canids was determined by its average percent contribution to the neously. The total presences available (N = 1187) were intersected models. The relation between occurrence of canids and EGVs was with the EMs to calculate the percentage of correct classification of determined by the visual examination of response curves profiles presences in each of the three probability categories for each spe- from univariate models (Austin, 1987; Phillips et al., 2006). Similar cies. Identification of areas of probable sympatry between pairs of profiles between two canids for a given EGV were taken as an indi- canids was determined by the overlap of the EMs using the ‘‘Raster cation of parallel relationships between the occurrence of these Calculator” function of ArcMap GIS. species and the range of variation of the EGV (Martínez-Freiría et al., 2008; Torres et al., 2009). This would indicate also the possi- 3. Results ble occurrence of sympatry and eventual competition within the range of values of the EGV equally selected by both species. Con- 3.1. Biogeographic patterns versely, a distinct profile of a canid in relation to others was taken as an indication of divergent relationships and possible spatial Six main topoclimatic units were identified by Principal Compo- exclusion (Martínez-Freiría et al., 2008). nents Analysis in the training area (Appendix S1), Humid (6.6% of the area), Arid (12.0%), Coastal (8.5%), Desert (51.3%), Sahel 2.5. Projection for North Africa and sympatry areas (17.1%), and Savanna (4.5%). There were significant differences (X2 = 555.2, df = 20; p < 0.001) in the percentage of pixels with Predictive models were projected to all North Africa by applying presences of canids among the identified topoclimatic units them to another set of environmental layers composed exactly of (Fig. 2), indicating that V. zerda and V. rueppellii were mostly found the same set of EGVs. Projecting models to a wider area may lead in the coastal and desert units, V. pallida only in Sahel and savanna to biases in predictions since environmental values and features units, V. vulpes mostly in humid and arid units, whereas C. aureus may fall outside the range of values encountered during model was found in all units. Bs measure of niche breadth was lower training (Phillips, 2008). Therefore, clamping maps depicting pro- for V. pallida and V. zerda, and higher for C. aureus indicating that jection pixels whose EGV values are outside of the range repre- the former were more specialised than the latter (Fig. 2). sented in the training area, were produced by Maxent for each species, and overlaid to identify areas of uncertainty in the projec- 3.2. Evaluation of models tion of Topoclimatic and Habitat models. To quantify areas of high probability for species presence and The ROC plots for the training dataset exhibited high average sympatry, models were reclassified to display areas of probable ab- AUCs of 0.919 and 0.867 for the Topoclimatic (TMs) and Habitat sence and presence for each species. Maxent models classifies (HMs) models built with the dataset of selective criteria for the squares with continuous values of probability of occurrence be- training area, respectively, whereas average AUCs for test dataset tween 0 and 1, thus it was necessary to determine the threshold were slightly lower, 0.913 and 0.797, respectively (Appendix S3). above which it is considered that the species is present. The tenth Differences in AUCs between models built randomly and using percentile training presence thresholds given by Maxent were cho- selective criteria were not significant neither for models built with Author's personal copy
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Fig. 2. Percentage of pixels with presence of canids in each topoclimatic unit defined by Principal Components Analysis in training area, availability of each topoclimatic unit and Standardised Levin’s B (Bs) measure of niche breadth. topoclimatic (F < 1.261; p > 0.623 in all cases) nor habitat variables Profiles of response curves for the EGV most related to the dis- (F < 1.553; p > 0.251 in all cases). There was a trend for TM (aver- tribution of species revealed similar patterns for groups of canids age: 0.921) to have higher AUCs than HM (average: 0.844) (Appen- (Fig. 3): (1) V. vulpes and V. zerda occur more frequently in areas dix S3). Nevertheless, these differences were only significant for with high temperature annual range, but the former above 30 °C the test dataset of the training area (F = 12.017; p = 0.0008). The and the latter only above 40 °C; (2) V. rueppellii and V. zerda occur following results are based in models developed only with selec- only in areas with less than 200 mm of annual precipitation and V. tive criteria. pallida with less than 600 mm; (3) V. zerda and V. rueppellii occur mostly in areas of stony desert; (4) C. aureus and V. vulpes are 3.3. Environmental factors related to species occurrence the only two species present in areas with annual precipitation above 600 mm and minimum temperature below À10 °C; and (5) The TM and HM developed for the training area allowed the dis- C. aureus, V. pallida and V. vulpes occur almost exclusively in areas tinction of EGV related to the distribution of canids (Table 2; of sparse grassland and distant from stony deserts. Appendix S4): C. aureus is mostly related to maximum tempera- In comparison with the remaining canids, specific patterns were ture, temperature annual range, close deciduous forests and sparse observed: (1) C. aureus occurs mostly in areas with annual precip- grasslands; V. pallida is related to precipitation of wettest month, itation above 1000 mm; (2) V. pallida occurs exclusively in areas minimum temperature and open grasslands; V. rueppellii is mostly with minimum temperature above 15 °C and in areas of open related to temperature annual range, annual precipitation, bare grassland distant from stony desert; and (3) V. vulpes only occurs rock, croplands and stony desert; V. vulpes is mostly related to min- in areas distant from open grasslands. imum temperature, annual precipitation and sparse grasslands; and V. zerda is related to temperature annual range, annual precip- 3.4. Predicted species occurrence itation and stony desert. There were common EGV related to the distribution of most canids, such as temperature annual range, Model predictions for all North Africa were classified into high minimum temperature, annual precipitation, sparse grasslands presence, moderate presence and absence probability. The average and stony desert. percentage of observations in areas of high probability of presence and absence was 72% and 5%, respectively, but rose to above 90% in
Table 2 all species, when areas of high and moderate probability of occur- Percent contribution of each variable for the Maximum Entropy models in the rence were combined (Table 3). training area built with topographical and climatic variables (Topoclimatic model), Areas of uncertainty in model projection for the training area to and with land-cover variables (Habitat model). Variables that sum at least 75% of all North Africa were almost absent from the Habitat models à contribution for each species are marked ( ). (Appendix S5). For the Topoclimatic models, there were several C. aureus V. pallida V. rueppellii V. vulpes V. zerda Average areas of uncertainty mostly located on the south-western and Topoclimatic model south-eastern limits of the projection area and also the central- SLOP 15.0à 3.3 1.8 3.0 4.7 5.6 western region of Algeria. TANR 29.4à 4.2 51.6à 7.6 49.9à 28.5 The projection of models for North Africa (Fig. 4; Appendix S6) à à TMIN 11.4 36.8 2.0 48.2 7.0 21.1 identified potential areas for the occurrence of C. aureus in almost TMAX 36.7à 0.1 4.2 14.4à 2.0 11.5 ANPR 5.4 2.2 38.2à 26.5à 25.8à 19.6 all North Africa with the exception of the extreme hyper-arid areas PWET 2.1 53.3à 2.2 0.2 10.6 13.7 of the Sahara: Majâbat al-Koubrâ in Mauritania-Mali, the Ténéré in Habitat model Niger, the Libyan and Western Deserts of Libya–Egypt, and the Nu- DEGFO 1.6 0.0 0.0 1.7 0.0 0.7 bian desert of Sudan–Egypt (more than 85% of North Africa corre- DCDFO 26.3à 0.0 0.0 2.2 2.9 6.3 sponding to nearly 824,000 km2; Table 4). Probable areas of à à DSHRU 10.7 1.5 10.0 14.4 0.9 7.5 occurrence of V. pallida were restricted (less than 15% correspond- DCLGR 4.1 0.0 2.7 9.8à 17.7à 6.9 ing to about 140,000 km2; Table 4) to a relatively narrow band DOPGR 2.3 88.3à 4.3 9.6 1.0 21.1 DSPGR 19.5à 9.5 14.3à 41.7à 5.0 18.0 along the Sahelian belt from Mauritania to Sudan–Eritrea and also DCROP 3.7 0.1 23.0à 1.1 2.1 6.0 in some isolated pixels in the southern Saharan mountains. Areas DSAND 12.3à 0.3 2.3 14.4à 6.2 7.1 of probable occurrence of V. rueppellii were identified for most à à à DSTON 10.4 0.1 16.9 3.0 57.3 17.6 of North Africa, but the canid is absent from the northern DBROC 10.0 0.3 26.5à 2.0 6.9 9.1 Mediterranean region, the savannas south of the Sahel and the Author's personal copy
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Fig. 3. Response curves for the topoclimatic (left) and habitat (right) environmental factors most related (with more than 15% on average of contribution to the model) to the distribution of canids in training area.
Table 3 Number and percentage (in brackets) of all observations of canids in each category of presence probability classified by the Ensemble Threshold model.
Absence Presence moderate Presence high Presence moderate and high N C. aureus 22 (5.0) 38 (8.7) 376 (86.2) 414 (95.0) 436 V. pallida 1 (2.5) 9 (22.5) 30 (75.0) 39 (97.5) 40 V. rueppellii 15 (8.6) 50 (28.7) 109 (62.6) 159 (91.4) 174 V. vulpes 23 (7.1) 55 (17.0) 246 (75.9) 301 (92.9) 324 V. zerda 6 (2.8) 83 (39.0) 124 (58.2) 207 (97.2) 213 Average (%) 5.2 23.2 71.6 94.8
Fig. 4. Probability of occurrence of North-African canids at a 9961 Â 9961 m scale estimated by Maximum Entropy using the ensemble of Topoclimatic and Habitat models (Ensemble Threshold model). Author's personal copy
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Table 4 Percentage of training (left) and projection (right) areas identified with high probability (both high and moderate presence probability) for the occurrence of canids according to the Topoclimatic and Habitat models, and identified as potential for species occurrence by the Ensemble Threshold models.
% High probability % Potential Topoclimatic model Habitat model Ensemble Threshold model C. aureus 59.4/52.7 82.1/80.8 85.8/85.7 V. pallida 17.5/13.0 9.2/7.4 17.8/14.6 V. rueppellii 62.8/39.7 57.3/58.2 75.9/69.1 V. vulpes 24.4/15.4 21.5/11.5 26.2/19.4 V. zerda 50.1/35.7 60.0/66.7 72.5/74.0
extreme hyper-arid areas (more than 69% corresponding to nearly or the stripped ground squirrel (Xerus erythropus)(Le Berre, 1989, 665,000 km2; Table 4). Probable areas of occurrence of V. vulpes 1990). These relict populations colonized this region at least during were also relatively restricted (less than 20% of North Africa corre- the Holocene, when the climate was more humid and the Sahara sponding to about 187,000 km2; Table 4) and identified in the much more reduced than in current times, and became isolated Mediterranean coastal areas, the Algerian Saharan Atlas and High with the increasing aridity that followed this period (Le Houérou, Plateaux, several isolated pixels corresponding mostly to the high- 1997). It can be hypothesised that V. pallida also colonized this re- er altitude areas of Saharan mountains, and also in some pixel gion during more humid climatic periods but it went extinct when along the Nile valley. Models for V. zerda exhibited major discor- aridity and probably competition with V. rueppellii and/or V. vulpes dances between TM and HM but there was a trend for areas of increased. Analysis of the fossil record is needed to clarify the his- probable occurrence being located in almost all the Sahara desert torical range of this canid. (nearly 75% corresponding to about 711,000 km2; Table 4) with Currently, there are V. vulpes populations along the Nile river the exception of small core areas of hyper-arid regions. from Egypt to Sudan, restricted to the river valley, benefiting from the man-made agricultural fields and settlements, and water avail- ability (Osborn and Helmy, 1980; Sillero-Zubiri et al., 2004). The 3.5. Predicted sympatry areas Topoclimatic model suggests that this region is highly unsuitable for the species, but the Habitat model identifies several suitable Probable sympatry between V. rueppellii and V. vulpes (Fig. 5 pixels along the river valley (about 1000 km2). Therefore, it can top) was identified along a relatively narrow stripe spreading from be hypothesised that the species was far more widespread during coastal southern Morocco to northern Egypt (10.3% of the study the humid Holocene and then it started retracting as Saharan arid- area corresponding to nearly 99,000 km2). This band is relatively ity increased, presenting currently a relict population along the riv- wide in Morocco (about 100 km) including the coastal region be- er banks. Further support for this hypothesis steams also from tween the Souss and Drâa river valleys, the southern slopes of ecological models suggesting that there are suitable pixels for the the Anti-Atlas and Drâa river valley, and in the region of Bou-Saada species in Sahara Mountains and along the Sahelian belt. In fact, – Biskra in Algeria (about 200 km wide), but it is very narrow (usu- Saharan mountains constitute refugia for several species of Medi- ally less than 40 km) along the Saharan Atlas in Algeria and in the terranean affinity, such as the false smooth snake (Macroprotodon Mediterranean coastal areas of Libya and Egypt. Potential sympatry cucullatus), and of sub-Saharan affinity, like the baboon (Papio between V. pallida and V. rueppellii (Fig. 5 bottom) was identified in cynocephalus)(Le Berre, 1989, 1990). Probably isolated populations several scattered regions along the Sahelian belt of Mauritania, of V. vulpes could still persist in the Hoggar, Aïr or Tibesti. Field sur- Chad and Sudan (3.8% of the study area corresponding to nearly veys are needed to confirm this hypothesis and molecular studies 37,000 km2). needed to reconstruct the evolutionary history of Nile river populations. 4. Discussion 4.2. Predicted species occurrence 4.1. Biogeographical patterns and environmental factors related to species occurrence Modelling separate components of the ecological niche allowed disentangling the importance of topoclimatic from habitat factors. All canids exhibited distinct biogeographical affinities which are Although the independent analyses of environmental factors is less reflected in the different habitat selection patterns found. For in- frequently applied than modelling all factors together (but see stance, V. rueppellii but especially V. zerda are mostly related to Pearson et al., 2004; Anadón et al., 2007), in this study it stressed the Desert topoclimatic unit of the study area and both species that certain regions can be suitable for the occurrence of a species only occur in driest areas, distant from open grasslands and close according to topoclimatic traits but not by habitat traits and vice to stony desert habitats. The affinity of V. pallida to the Sahel unit versa. Furthermore, it identified small-sized suitable habitat is also expressed by the most frequent occurrence in warm and hu- patches inside large climatically unsuitable areas; for instance, mid areas with moderate temperature annual range. C. aureus and the rock outcrops of the Mauritanian Adrar Atar and Tagant are V. vulpes are the only two canids occurring in the Humid unit and suggested as exhibiting suitable habitat for the occurrence of C. concurringly the only two present in the most humid and cold re- aureus but are located in a climatically unsuitable area (Appendix gions of the study area. S6). Biogeographical inferences can be made from the ecological Areas of probable occurrence identified for North Africa follow models. For instance, few pixels with suitable climate (about the general distribution patterns previously identified for these ca- 170 km2) are identified for V. pallida in the coastal region between nids (Sillero-Zubiri, 2009). Nevertheless, fine-scaled ecological the Souss and Drâa river valleys, south-western Morocco, in a re- models allowed the definition of accurate suitable habitats for spe- gion almost 1500 km to the north of the species range. Interest- cies that were previously considered widespread. For instance, the ingly, this region currently holds isolated populations of several ensemble threshold models suggest that probable occurrence species of sub-Saharan affinity, like the puff adder (Bitis arietans) areas for C. aureus and V. rueppellii are mostly located in Saharan Author's personal copy
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Fig. 5. Areas of probable sympatry between V. rueppellii and V. vulpes (top) and between V. rueppellii and V. pallida (bottom) in North Africa, at a 9961 Â 9961 m scale, according to the ensemble threshold models. Three classes of probable sympatry are considered: pixels of high occurrence probability for both species (sympatry), pixels with high probability for one species and intermediate for the other (>/<), and all remaining pixels (no sympatry). peripheral areas with fragmented populations in mountains, and as belonging to the category ‘‘Sandy Desert” probably by radiomet- that unsuitable areas for species presence occur in sand seas and ric saturation of sensors, which occurs in desert transition zones hyper-arid regions. Spatial bias in sampling effort could have (Karnieli et al., 2004). Nevertheless, the habitat model suggests caused lack of prediction in inland arid regions, but ecological that the species is positively related to presence of stony desert models were apparently robust. For instance, the unsampled (the desertic habitat with highest availability in the study area), Majâbat al-Koubrâ is predicted to have suitable habitats for capturing the essential desertic nature of the habitats where this V. zerda but not for C. aureus and V. rueppellii, and in fact the former canid dwells. was recorded in this region whereas the later pair of canids was Observations selected for the test dataset included many uncer- suggested to be absent (Monod, 1996). tain presences (old records, tracks and faeces), which could prevent The ecological model for V. zerda had lower AUC in comparison model testing with an adequate independent dataset. However, the with the remaining canids and spatial artefacts in the prediction of average AUC for the test data was high (0.855; Appendix S3) and potential distribution. V. zerda is found almost exclusively in sandy the percentage of uncertain test presences in high suitability pixels habitats, ranging from large sand seas (erg) to small sandy patches ranged from 94% (V. rueppellii) to 100% (V. pallida, V. vulpes and V. over rocky terrain (Cuzin, 2003; Sillero-Zubiri, 2009). Pixels corre- zerda). The selective criteria used apparently allowed ecological sponding to small-sized ergs were not identified by remote sensing models to evaluate the reliability of dubious records. For instance, Author's personal copy
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V. pallida has been cited from the regions of Dongola, Sudan (Set- the complete range of species like V. pallida. Furthermore, this zer, 1957); Erg Admer, Algeria (Lavauden, 1926) and Tibesti, Chad study assessed the world distribution of V. pallida at a scale suit- (Le Berre, 1990). These northernmost observations result most able for defining its conservation status (Sillero-Zubiri, 2009). likely from misidentifications with V. rueppellii (Kowalski and Rze- Road mortality was previously unknown for V. pallida and V. bik-Kowalska, 1991), and this study further suggests these regions rueppellii (Sillero-Zubiri et al., 2004), but this study demonstrates as unsuitable. On the contrary, few pixels of suitable habitat (about that roads can be an important source of mortality for North-Afri- 90 km2) where identified for V. pallida in the Aïr mountains, Niger, can canids. About 8.5% (N = 53) of the observations of canids from where fragmented populations are known to occur (Dekeyser, the training area came from road-killed specimens and 47% 1950). (N = 15) of the observations of V. pallida were collected along the road connecting Nouakchott and Nema (Mauritania). Another haz- 4.3. Areas of probable sympatry ardous road for canids is located along the littoral of Western Sa- hara, where 30% (N = 16) of road-killed specimens were observed Ecological models predicted potential sympatry between V. vul- including C. aureus, V. rueppellii, and V. zerda. The impact of road pes and V. rueppellii in areas where both species are known to pres- mortality on population dynamics remains unclear, but the ent contact zones. Field observations in the lower Drâa valley increasing complexity of road networks will most likely intensify suggested that V. vulpes is found in areas close to productive envi- the negative effect of road killing on canid populations in the fol- ronments with water availability whereas V. rueppellii is restricted lowing decades. to the less productive Saharan environments (Cuzin, 2003). Ecolog- This study demonstrates that several canids have suitable hab- ical models support these observations: V. rueppellii is mostly itats along the Mediterranean Basin biodiversity hotspot, but also found in areas with low precipitation and at short distances to stressed the Sahara as important for their long-term conservation. stony desert while V. vulpes is found in areas with high precipita- Deserts have overall low richness, and thus are not ranked as bio- tion and at longer distances. Nevertheless, models predict a rela- diversity hotspots, but they can have high local diversity (reviewed tively wide band of sympatry between these canids in south- by Ward 2009). Their large extent and bareness allows trans-fron- western Morocco which is not supported by field observations (Cu- tier management of species and key-habitats may give refuge for zin, 2003). This suggests that although topoclimatic and habitats certain highly endangered species. In fact, the biological value of traits of the area are suitable for both species, in fact, competition Saharan mountains is emphasised as they constitute suitable areas is probably leading to spatial exclusion. Probably, these canids for all studied species. These isolated ‘‘continental-islands” may compete for both prey and den sites (Sillero-Zubiri et al., 2004), constitute refugia for canids under climate change scenarios as but apparently V. vulpes is capable of displacing V. rueppellii since they do already for numerous plant and animal species (Quézel, it is the most frequently found canid inside the predicted sympatry 1978; Le Berre, 1989, 1990; Trape, 2009). Future field surveys de- area (Cuzin, 2003). Actually, V. rueppellii is on the verge of extinc- signed for the quantification of biodiversity levels in these moun- tion in the Negev Desert, Israel, due to competitive exclusion by V. tains are urgently needed. vulpes (Yom-Tov and Mendelssohn, 1988) and it is known also to Distribution and habitat selection patterns observed in this be displaced in the Arabian peninsula (reviewed by Sillero-Zubiri, study may give indications about the mid-sized Saharan carnivore 2009). Future expansion of V. vulpes could probably occur along guild. Probably, other carnivores with circum-Saharan range (e.g. the climatically-mild Western Sahara, due to the recent settle- caracal, Caracal caracal), with isolated populations in mountains ments that have been installed along the major paved route of (e.g. Saharan striped polecat, Ictonyx libycus) or with strict-Saharan the region (authors, pers. observ.). range (e.g. sand cat, Felis margarita) should evidence similar envi- Ecological models predicted fragmented pixels of potential ronmental responses and extinction risks as the canids studied. sympatry between V. pallida and V. rueppellii along the Sahel. Re- Finally, ecological-niche based models, combining high resolu- sponse curves profiles suggest that high temperature annual range tion environmental factors and presence data, can be applied to and large distance to stony deserts and open grasslands obstructs other remote regions of the world and should be developed for the contact of V. pallida with V. rueppellii, whereas low levels of an- other Saharan large mammals with rare and scattered records. nual precipitation and relatively short distances to stony deserts The methodological approach of this study should be applied to facilitates sympatry between these species. Sympatry between the highly endangered North African populations of addax (Addax these species should only occur in areas with annual precipitation nasomaculatus), dama gazelle (Gazella dama), cheetah (Acinonyx between 100 and 200 mm, which are precisely the rainfall levels of jubatus) and African wild dog (Lycaon pictus) to ascertain their sta- Tagant mountains. In these mountains, V. pallida is frequently tus and identify key-areas for conservation management. found in lowland sandy areas whereas V. rueppellii in rock–sand substrates at higher altitudes and localities of strict sympatry re- Acknowledgments main to be found (authors, pers. observ.). Clearly, ecological studies of contact zones between V. pallida, V. rueppellii and V. vulpes are This study was partially supported by two grants from National needed in order to quantify driving-forces of spatial coexistence/ Geographic Society (7629-04 and 8412-08). JCB has a contract exclusion. Furthermore, studies with molecular markers would (Programme Ciência 2007) from Fundação para a Ciência e Tecno- contribute to the understanding of evolutionary relationships and logia (Portugal). Logistic support for overland expeditions was gi- to detect possible hybridization. ven by Trimble, Off-Road Power and the Parc National du Banc d’Arguin (Mauritania). Acknowledgments extended to the numer- 4.4. Conservation implications ous researchers who gave unpublished observations and to R. God- inho from CIBIO/UP (Portugal) for species diagnosis of several road- This study presents new data on the observed distribution of ca- killed specimens using genetic markers. The manuscript was nids in North Africa at high resolution scale. The compilation of greatly improved by the comments of two anonymous referees. data scattered over many local-scale reports and studies allowed the production for the first time of relatively precise species distri- Appendix A. Supplementary material bution maps for both the training area (roughly 2 Â 2 km) and all North Africa (roughly 10 Â 10 km). Precise distribution maps for Supplementary data associated with this article can be found, in all canids were unavailable for countries like Mauritania or for the online version, at doi:10.1016/j.biocon.2009.08.001. Author's personal copy
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TM Dataset Average TMs selective Training AUC 0.853 0.954 0.916 0.941 0.928 0.919 Test AUC 0.851 0.960 0.940 0.885 0.927 0.913 TMr random Training AUC 0.864 0.958 0.922 0.937 0.945 0.925 Test AUC 0.870 0.967 0.942 0.919 0.931 0.926
HM Criteria Average HMs selective Training AUC 0.789 0.966 0.831 0.931 0.820 0.867 Test AUC 0.759 0.814 0.761 0.895 0.754 0.797 HMr random Training AUC 0.785 0.969 0.832 0.921 0.796 0.860 Test AUC 0.815 0.945 0.843 0.921 0.742 0.853