Environmental Conservation 37 (2): 1–8 © Foundation for Environmental Conservation 2010 doi:10.1017/S0376892910000214

1 Land-use changes as a critical factor for long-term wild rabbit 2 conservation in the

∗ 3 MIGUEL DELIBES-MATEOS1,2 ,MIGUEL ANGEL´ FARFAN´ 1,3,JESUS´ OLIVERO1 AND 4 JUAN MARIO VARGAS1 5 1Departamento de Biolog´ıa Animal, Facultad de Ciencias, Universidad de Malaga,´ 29071 Malaga,´ 2Instituto de Investigacion´ en Recursos 6 Cinegeticos,´ IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071 Ciudad Real, Spain and 3Biogea Consultores, C/Navarro Ledesma, 7 243, 29010 Malaga,´ Spain 8 Date submitted: 17 September 2009; Date accepted: 27 January 2010

9 SUMMARY INTRODUCTION 44 10 European rabbits (Oryctolagus cuniculus), a multi- European wild rabbits (Oryctolagus cuniculus), are considered 45 11 functional keystone species in the Iberian Peninsula, a multifunctional keystone species in the Iberian Peninsula 46 12 have drastically declined over past decades. Rabbit (Delibes-Mateos et al. 2007). Rabbits conspicuously alter 47 13 decline has been frequently attributed to the arrival landscapes and provide foraging, shelter and nesting habitats 48 14 of two viral diseases. However, decline was apparently for a diverse array of species, their grazing activities alter 49 15 ongoing before the arrival of the diseases, apparently plant species composition and vegetation structure, especially 50 16 as a consequence of habitat loss and fragmentation. by creating open areas and preserving plant species diversity, 51 17 In this paper, the effect on rabbit populations of and they are prey for a large number of predators (Delibes- 52 18 land-use changes during recent decades in Mateos et al. 2008a;Galvez-Bravo´ et al. 2009). 53 19 (southern Spain) is analysed. Areas favourable for Rabbits have massively declined in the Iberian Peninsula 54 20 rabbits both at present and during the 1960s are since the first half of the 20th century, and this is frequently 55 21 identified, and the environmental and land-use factors attributed to the arrival of the viral diseases myxomatosis from 56 22 that determine these areas established. In areas 1953, and rabbit haemorrhagic disease (RHD) from 1988. 57 23 where the favourability for rabbits has changed However, rabbit decline was already ongoing in the first half 58 24 during recent decades, main land use changes are of the 20th century, apparently as a consequence of habitat loss 59 25 assessed to identify possible factors explaining rabbit and fragmentation (Ward 2005). Rabbits populations declined 60 26 favourability in these areas. Areas favourable to in Spain by 73% between 1973 and 1993 and this decline was 61 27 rabbits are currently determined by factors similar by no means restricted to the period 1988–1993 (Virgos´ et al. 62 28 to those during the 1960s; these areas have undergone 2007), when RHD was becoming widely established. Other 63 29 geographic changes in recent decades, apparently factors such as habitat loss are evidently also involved in the 64 30 as a consequence of land-use changes in Andalusia. decline of rabbits. The decrease in rabbit numbers may have 65 31 The percentages of the variables that were positively had important cascading effects on the functioning of the 66 32 associated with rabbit favourability in both models Iberian Mediterranean ecosystem, with serious ecological and 67 33 (current and 1960s) have declined in Andalusia as a economic consequences (Delibes-Mateos et al. 2008a). 68 34 whole, and in areas where rabbit favourability has Researchers have therefore made great efforts to study 69 35 decreased; hence environments suitable for rabbits the main causes of rabbit population decline in the Iberian 70 36 have become impoverished. Conversely, in both Peninsula; the number of research papers focused on this 71 37 models, environments suitable for rabbits increased species has significantly increased in the Iberian Peninsula 72 38 in municipalities, where rabbit favourability also following the population decline (Piorno 2006). Most of 73 39 increased. The preservation of rabbit-friendly habitats this research effort has focused on diseases. However, and 74 40 should be a priority for the conservation of this key although many studies have addressed the relationships 75 41 species in the western Mediterranean. between habitat characteristics and the distribution and 76 42 Keywords: agricultural intensification, favourability function, abundance of rabbit populations in the Iberian Peninsula (for 77 43 habitat loss, land abandonment, Oryctolagus cuniculus example Calvete et al. 2004; Fernandez´ 2005), information 78 on the effects of habitat loss on Iberian rabbit populations 79 is scarce. In general, nearly all studies have focused on the 80 association of recent rabbit abundances and/or trends with 81 present landscape features (for example Calvete et al. 2006), 82 whereas there are no studies on this relationship several 83 decades ago. In fact, past information on rabbit abundance 84 ∗Correspondence: Dr Miguel Delibes-Mateos Tel: +34 952131861 has never been used in previous studies. Therefore, it is very 85 Fax: +34 952131668 e-mail: [email protected] difficult to know how landscape changes have affected rabbit 86 2 M. Delibes-Mateos et al.

2006). Using this approach, we evaluated whether rabbit 108 habitat requirements may have changed in recent decades. 109 Alternatively, we identified areas where the favourability for 110 rabbits has markedly changed (either increased or decreased) 111 during recent decades, and evaluated the evolution of the 112 main land use that explains rabbit favourability in these areas, 113 as well as in the whole study area. We also discuss how land- 114 use changes have affected rabbit distribution and abundance 115 in recent decades in the western . 116

METHODS 117 Study area 118 Andalusia covers more than 87 000 km2 in the southernmost 119 part of mainland Spain, and is administratively divided into 120 771 municipalities. The main mountain ranges are the Sierra 121 Morena, along the northern fringe of the , and the 122 Baetic System, sub-divided into two ranges, Sub-baetic and 123 Penibaetic, which are oriented NE–SW and mainly occupy 124 the eastern part of the region. The most important plain is the 125 valley, which is longitudinally oriented between 126 the and the Baetic System (Fig. 1). Andalusia 127 has a Mediterranean climate, with mild winters and severe 128 summer droughts (see Delibes-Mateos et al. 2009a for a wider 129 description of the study area). 130

Variables 131

Figure 1 Study area. The main mountain ranges (Sierra Morena Andalusian municipalities were assigned to groups according 132 and the Baetic System, sub-divided into two ranges, Sub-baetic and to whether rabbits were relatively abundant or not at present 133 Penibetic) and the most important valley (Guadalquivir valley) are and during the 1960s, using information from current hunting 134 shown in schematic form. Limits between provinces are also yields (1993–2001) and from game species abundance maps 135 indicated. available from the Mainland Spanish Fish, Game and National 136 Parks Service, respectively. 137 We analysed 32 134 annual hunting reports (AHRs) from 138 87 populations, and how such changes have contributed to rabbit the period 1993–2001 reported by 6049 game estates to 139 88 decline in the Iberian Peninsula. estimate the average hunting yields of the abovementioned 140 89 In Andalusia (southern Spain; Fig. 1), where rabbits species in each Andalusian municipality (n = 771), according 141 90 have traditionally reached high densities (Villafuerte et al. to the following equation: 142 91 1998), land use has changed substantially over recent decades  mean annual number of individuals hunted pergame estate 92 (Fernandez-Al´ es´ et al. 1992). Economic growth and the rural HY =  93 exodus have led to the intensification of agriculture and areas of the game estates 94 livestock farming in certain areas, and to the under-use of ×100 95 other vast rural areas (Fernandez-Al´ es´ et al. 1992). Both 96 processes have destroyed large areas of traditional agricultural where HY is the hunting yield per municipality expressed 143 97 landscapes, where rabbits usually reach their highest densities by the number of individuals captured per 100 ha of game 144 98 (Calvete et al. 2004). We suspect that the drastic changes in estate where the species is hunted (Vargas et al. 2007). 145 99 land use (Fernandez-Al´ es´ et al. 1992) must have affected the The Mainland Spanish Fish, Game and National Parks 146 100 rabbit distribution and abundance in Andalusia. Service made abundance maps for each game species by using 147 101 In this paper, our main aims were to identify areas in estimated hunting yields in the 1960s. These maps, whose 148 102 Andalusia that are favourable for rabbits at present and during scale is 1:2 000 000, indicate the abundance of the main game 149 103 the 1960s, and to establish the environmental and land use species throughout Spain on a 1–6 scale (where 1 = absent, 2 = 150 104 factors that determine these areas in both periods. We define rare, 3 = scarce, 4 = frequent, 5 = abundant and 6 = very 151 105 favourable areas as those where the environment increases abundant; Ministerio de Agricultura 1968; see also Gortazar´ 152 106 the probability of presence of rabbits, independently of the et al. 2000; Delibes-Mateos et al. 2009a). Using this 153 107 proportion of area they occupy (‘prevalence’; see Real et al. information, we extracted the mean value of wild rabbit 154 Land-use changes: a risk for rabbit conservation 3

Table 1 Variables used to model the potential distribution of as well as for the 1960s, when the abundance value was lower 164 wild rabbit abundance in south-Iberian municipalities. Sources: than 4. IA was then used as a target variable in the modelling 165 1 2 US Geological Survey (1996); derived from GlobDEM50 (Farr procedure. 166 3 & Kobrick, 2000); Mapa de usos y coberturas vegetales del suelo We related the IA to 27 predictor variables that provided 167 de Andaluc´ıa (1956, 1999). information on the environmental characteristics, land use 168 Variables Code and vegetation in the Andalusian municipalities (Table 1). 169 Orographic Altitude (m) 1 ALTI Orographic variables were derived from US Geological 170 1 Slope (%) SLOP Survey (1996), and GlobDEM50 (Farr & Kobrick, 2000), 171 2 Exposure to the south SE whereas natural vegetation and crops variables were obtained 172 2 Exposure to the west WE from Mapa de usos y coberturas vegetales del suelo de 173 Natural Built land (% area) 3 BL Andaluc´ıa (Junta de Andaluc´ıa 1956, 1999). Exposure to the 174 vegetation south and exposure to the west (the SE and WE variables) were 175 Wetlands (% area) 3 WETL Pasture (% area) 3 PAST derived from GlobDEM50 high-resolution digital elevation 176 Oak wood (% area) 3 OAKW data, based on raw data from the Shuttle Radar Topography 177 Pasture with oaks (% area) 3 PWO Mission (SRTM; Farr & Kobrick 2000). To this end, we used 178 Pasture with conifers PWC the spatial analyst toolbox of ArcMap. We calculated a 90 × 90 179 (% area) 3 m resolution aspect map with surface analysis, and from this 180 Dense scrub with oaks DSWO we extracted the degree of exposure to the south and west, 181 3 (% area) respectively. Thus, for variable SE, a pixel whose aspect is 182 3 Sparse scrub (% area) SS south was given the value 180, a pixel whose aspect is north 183 Sparse scrub with oaks SSWO was given the value 0, and pixels with intermediate aspects 184 (% area) 3 were given intermediate values. The procedure was analogous 185 Dense scrub with conifers DSWC for variable WE. More details in relation to the process used 186 (% area) 3 Sparse scrub with conifers SSWC to obtain the rest of the orographic, natural vegetation and 187 (% area) 3 crop variables included in Table 1 are provided in Vargas 188 Sparse scrub with diverse trees SSWD et al. (2007). 189 (% area) 3 Dense scrub with diverse trees DSWD Predictive models 190 (% area) 3 3 Conifer wood (% area) CW To select a subset of significant predictor variables, we 191 3 Dense scrub (% area) DS performed stepwise logistic regression (Hosmer & Lemeshow 192 Crop Irrigated herbaceous crops IHER 1989) of IA on the predictor variables, using SPSS 193 (% area) 3 14.0 statistical software. We then used the environmental 194 Irrigated woody crops IWC favourability function of Real et al. (2006) to eliminate from 195 (% area) 3 Dry herbaceous crops (% DHER the model the effect of the uneven proportion of ones and 196 area) 3 zeros in the dataset. The favourability for a positive IA in each 197 Dry heterogeneous crops DHET municipality was obtained from the formula: 198 (% area) 3 Irrigated heterogeneous crops IHET F = (P/(1 − P))/((n1/n0) + (P/(1 − P))) (% area) 3 3 Dry wood crops (% area) DWC where P is the probability value given by logistic regression, 199 Mosaic of crops and natural MCNV and n1andn0 are the number of municipalities with IA equal to 200 3 vegetation (% area) 1 and 0, respectively (Real et al. 2006). This function provided 201 Herbaceous crops with oaks HCWO a description of local deviations from the overall probability 202 (% area) 3 of obtaining good abundances. Thus, a value F > 0.5 meant 203 that the probability of an IA = 1 (anticipated owing to local 204 environmental conditions) was higher than that expected only 205 155 abundance in each municipality following the procedure according to the IA = 1/IA= 0 ratio (namely the reported 206 156 described in Delibes-Mateos et al. (2009a). IA = 1 prevalence in the territory). 207 157 As our aim was to detect areas favourable to rabbits, we To obtain an explanatory model, the variables introduced 208 158 followed the criterion of Farfan´ et al. (2004) and Vargas et al. in the final predictive model were grouped into orographic, 209 159 (2006) to estimate where the abundance of this species was natural vegetation and crop factors (Table 1), and each group 210 160 good (index of abundance, IA = 1) or poor (IA = 0). In this of variables was used to obtain partial orographic, natural 211 161 way, IA = 1 for the present period, when HY > 20, as well vegetation and crop favourability models. To take into account 212 162 as for the 1960s, when the abundance value was 4 or higher. the effect not explained by a single factor, which often 213 163 In contrast, IA = 0 for the present period when HY ≤ 20, results in an overlaid effect in space owing to collinearity 214 4 M. Delibes-Mateos et al.

215 between them (Borcard et al. 1992; Legendre 1993), we Table 2 Favourability models including coefficients of variables 216 performed a variation partitioning procedure to specify how in the favourability functions. The Wald parameter indicates the = 217 much of the variation of the final model was explained by relative importance of each variable. p statistical significance. 218 the pure effect of each explanatory factor, which proportion Year Variable Coefficient Wald p 219 was an indistinguishable effect of more than a single factor 1960s Slope −0.187 56.266 <0.001 220 (intersection) and how these factors interacted and affected Sparse scrub with 5.696 24.274 <0.001 221 the distribution of the wild rabbit abundances (Legendre 1993; oaks 222 Legendre & Legendre 1998; see an application in Farfan´ et al. Dry woody crop 2.442 33.198 <0.001 < 223 2008). Mathematically, negative intersections between factors Pasture 5.157 10.460 0.01 < 224 can appear, which measure the amount by which the effect of a Sparse scrub 1.896 10.008 0.01 Exposure to the west −0.0164 7.364 <0.01 225 factor is obscured by another factor through interrelationships Dense scrub with 7.414 6.194 <0.05 226 between variables (Cartron et al. 2000; Barcena´ et al. 2004). diverse trees 227 Municipalities with high, low or intermediate environ- Wetlands 2.889 4.478 <0.05 228 mental favourability for rabbits were defined according Exposure to the south 0.0102 3.966 <0.05 229 to a classification threshold. We considered favourable all Constant −0.254 230 municipalities whose favourability was 0.8 or higher, that Current Dry woody crop 2.624 45.004 <0.001 231 is, where the odds of good abundance were at least 4:1 Pasture 10.697 16.549 <0.001 232 (Rojas et al. 2001; Munoz˜ & Real 2006). Municipalities whose Slope −0.120 15.564 <0.001 233 favourability was 0.2 or lower were considered unfavourable Sparse scrub with 4.048 9.970 <0.01 234 (maximum odds 1:4), and favourability values between 0.2 oaks − < 235 and 0.8 were considered intermediate. We then compared Exposure to the south 0.0148 7.782 0.01 Altitude −0.000967 7.469 <0.01 236 the two models for the two periods that represented those Herbaceous crops −9.479 4.654 <0.05 237 municipalities where favourability was high in the 1960s and with oaks 238 now, where this was low in the 1960s and now, and where Sparse scrub 1.249 4.649 <0.05 239 favourability had changed from high to intermediate (F-I), Constant 0.920 240 from intermediate to low (I-U), from low to intermediate (U- 241 I) and from intermediate to high (I-F). Changes in the areas 242 dedicated to the different land uses within every municipality 243 were calculated as percentages (according to the Mapa de to the intersection between natural vegetation and crops after 269 244 usos y coberturas vegetales del suelo de Andaluc´ıa; Junta de excluding the effect of orography, as well as the effect owing to 270 245 Andaluc´ıa 1956, 1999), and then we quantified the changes in the intersection between orography and crops after excluding 271 246 every land use within the F-I, I-U, U-I and I-F areas. the effect of natural vegetation. At present, the intersection 272 between factors shows the same pattern as in the 1960s, 273 except for the effect due to the intersection between orography 274 247 RESULTS and natural vegetation, which has changed from negative to 275 248 The variables included in the logistic regression models, positive (Fig. 3). 276 249 ranked according to their order of entrance in each model Figure 4 shows the municipalities where favourable and 277 250 (Table 2) included six variables that were common to unfavourable conditions for wild rabbits have remained 278 251 both models, representing 66% and 75% of the variables stable from the 1960s to now, and where these conditions 279 252 included in the 1960s and the current models, respectively. have changed. Some municipalities have changed toward 280 253 According to these models, municipalities in Andalusia judged more favourable conditions (Fig. 4a). Thus, in the western 281 254 as favourable for rabbits tend to be aggregated (Fig. 2). In and central region of Andalusia, favourability increased 282 255 the 1960s, the most favourable areas for wild rabbit were from intermediate to favourable, whereas in the eastern 283 256 mainly located in the western part of the Sierra Morena and region this improved from unfavourable to intermediate. 284 257 Guadalquivir valley. However, currently favourable areas are Other municipalities have changed toward more unfavourable 285 258 located along the Guadalquivir slope of the Sub-baetic System conditions (Fig. 4b). Changes in favourability from favourable 286 259 and less mountainous of the western part of the Baetic to intermediate are concentrated in the middle of the western 287 260 System (Fig. 2). Andalusia, and changes from intermediate to unfavourable 288 261 The relationships between the explanatory factors were mainly in the eastern region. 289 262 complex (Fig. 3). In the 1960s, the effect owing to the Municipalities where favourable and unfavourable 290 263 intersection of orography, natural vegetation and crops was conditions for rabbits changed between the 1960s and present 291 264 positive, and the characteristics of factors that favour good day showed substantial changes in the percentage of surface 292 265 abundances tended to be present simultaneously. However, area occupied by vegetation types included in the favourability 293 266 the effect owing to the intersection between orography and models (Table 3). Thus, the percentages of surface area 294 267 natural vegetation was negative after excluding the effect of occupied by dry woody crops, pasture, sparse scrub with 295 268 crops; this was also the case regarding both the effect owing oak and sparse scrub have decreased in Andalusia since the 296 Land-use changes: a risk for rabbit conservation 5

Figure 2 Favourability values for good wild rabbit abundances in the municipalities of Andalusia, shown on a scale ranging from 0 (white) to 1 (black). Figure 3 Variation partitioning of the final model. Values shown in the diagrams are the percentages of variation in good abundance 297 1960s. Nevertheless, in the municipalities where conditions explained by the factors orography, natural vegetation and crops 298 favourable for rabbits have increased, the percentage of and by their interactions. 299 surface area occupied by these vegetation types has increased. 300 The percentage of herbaceous crops with oaks increased in 301 Andalusia since the 1960s. However, in the municipalities (Fernandez-Al´ es´ et al. 1992) could explain the geographical 317 302 where favourable conditions increased, the percentage of differences in rabbit favourability between the two study 318 303 surface area occupied by this vegetation type decreased, periods. 319 304 whereas in the municipalities where favourable conditions As regards the first hypothesis, our results suggest that 320 305 decreased, the percentage of surface area occupied by this favourable areas for rabbits are currently determined by 321 306 vegetation type increased. environmental and land-use factors similar to those of the 322 1960s; this is supported by the fact that six variables were 323 repeated in both favourability models (Table 2). Thus, as in 324 307 DISCUSSION the 1960s, favourable areas for rabbits are currently associated 325 308 The location of areas favourable for rabbits in Andalusia with the main habitat requirements for this small mammal: 326 309 has changed substantially over recent decades. In fact, we the presence of suitable food types (for example dry crops 327 310 have recorded an increase in favourability (especially from and pastures; Calvete et al. 2004; Fernandez´ 2005), and the 328 311 intermediate to favourable) in the areas that are currently availability of some form of cover for protection against 329 312 favourable for the species, and a favourability decrease in areas predators (such as sparse Mediterranean scrubland; Moreno 330 313 that were favourable for the lagomorph during the 1960s. Two & Villafuerte 1995). Moreover, land slope was negatively 331 314 hypotheses may explain these changes in favourability. First, associated with rabbit favourability during both study periods, 332 315 rabbit habitat requirements could have changed in recent which is not surprising given that rabbits typically avoid 333 316 decades. Second, recent changes in land use in Andalusia sloping mountain areas (Farfan´ et al. 2008). In only one of 334 6 M. Delibes-Mateos et al.

Table 3 Increase in the percentage of surface area occupied by land use and vegetation types included in the favourability models. I-F: municipalities where the environment has changed from intermediate to favourable for the wild rabbit; U-I: from unfavourable to intermediate; F-I: from favourable to intermediate; I-U: from intermediate to unfavourable. Included Andalusia I-F, U-I F-I, I-U in models 1960s and Dry woody crop −4.3 17.3 −19.4 current Pasture −14.9 33.5 −66.7 Sparse scrub with −0.6 66.5 −30.6 oaks Sparse scrub −15.1 3.1 −17.3 1960s Dense scrub with 7.0 −67.8 −43.1 diverse trees Wetlands −4.7 −3.4 −5.4 Current Herbaceous crops 60.0 −45.8 162.7 with oaks

335 the models, a few less statistically significant land use variables 336 were retained. For instance, dense scrub with diverse trees was 337 associated with areas favourable to rabbits during the 1960s, 338 but not at present (Table 2). Small patches of dense scrubland 339 were interspersed with pastures and crops several decades 340 ago in Andalusia (Fernandez-Al´ es´ et al. 1992), and therefore 341 rabbits could find refuge and food in this type of landscape. 342 Similarly, herbaceous crops with oaks were only present Figure 4 Municipalities where favourable and unfavourable 343 in the current favourability model (Table 2). This habitat conditions for a high abundance of wild rabbits have remained stable from the 1960s to now (black and light grey, respectively), 344 was negatively associated with favourable areas for rabbits and where these conditions have changed (dark grey). (a)Darkgrey 345 (Table 2), apparently because it offers high food availability indicates change toward more favourable conditions: either from 346 but little refuge protection for the species (Lombardi et al. intermediate to favourable (I-F zone), or from unfavourable to 347 2003). The area devoted to herbaceous crops significantly intermediate (U-I zone); (b) dark grey indicates change toward less 348 increased in recent decades (Table 3; see also Fernandez-´ favourable conditions: either from favourable to intermediate (F-I 349 Ales´ et al. 1992), which could explain why this habitat type zone), and from intermediate to unfavourable (I-U zone). 350 was only significant in the present day favourability model Thresholds for favourable and unfavourable areas are 0.8 and 0.2, 351 (Table 2). The possibility that rabbits have changed their respectively. 352 habitat requirements in the current landscape configuration 353 of southern Iberia is not totally excluded by coincidences in 354 the model, as the internal relationships between the variables and become positive (Fig. 3), probably because natural veget- 372 355 that are common to both models (their coefficients and order ation landscapes favourable for rabbits are presently confined 373 356 of importance according to the Wald’s parameter) are not to certain orographic zones. Specifically, the most suitable 374 357 identical. natural habitats are now mainly situated on the Guadalquivir 375 358 The partial orographic, natural vegetation and crop models slope of the Sub-baetic system and the western hills of the 376 359 show that orography is the most important factor explaining Penibaetic system (Fig. 2), which are regions with moderate 377 360 the distribution of wild rabbit abundance in Andalusia slopes that are also orographically favourable for rabbits. 378 361 (Fig. 3). In the 1960s, the types of natural vegetation landscape As habitat requirements for rabbits do not seem to have 379 362 that favoured the presence of rabbits were more widely changed, the most plausible explanation for the changes 380 363 distributed throughout the study area (Fernandez-Al´ es´ et al. observed in rabbit favourability would be the land-use changes 381 364 1992) and, as a consequence, orography may have been a more in Andalusia in recent decades. In agreement with this, we 382 365 limiting factor for this species than natural vegetation. Negat- suggest that the changes in landscape have been mainly 383 366 ive intersection between natural vegetation and crops during detrimental to rabbits during the study period. Thus, the 384 367 the 1960s (Fig. 3) means that the favourable natural vegetation percentages of the four habitat variables that were positively 385 368 conditions tend not to coincide with the favourable crop associated with rabbit favourability in both models (current 386 369 conditions when orography remains constant. After the 1960s, and 1960s; Table 2) have declined in Andalusia as a whole and 387 370 the partial importance of orography and natural vegetation de- in areas where rabbit favourability has decreased (Table 3; 388 371 creased, whereas the weight of their intersection has increased but see also Fig. 4b); hence, habitat suitable for rabbits has 389 Land-use changes: a risk for rabbit conservation 7

390 become impoverished. The reduction in woody crops and the data between the two study periods, we transformed the 445 391 pastures may have led to a decline in the availability of food original data into a binomial variable (good and poor areas 446 392 for rabbits in these areas (Calvete et al. 2004). Similarly, the for rabbit) that was directly comparable between both study 447 393 loss of sparse scrubland, mainly as a consequence of rural dates. 448 394 abandonment (Fernandez-Al´ es´ et al. 1992), has significantly There is a widely-held perception that all lagomorphs 449 395 reduced rabbit numbers in some areas in Andalusia (Moreno are fecund and are sufficiently generalist in their to 450 396 & Villafuerte 1995). Moreover, the increase in both dense overcome environmental changes. However, approximately 451 397 scrubland and herbaceous crops in Andalusia (Table 3) seems a quarter of all lagomorphs are threatened with extinction 452 398 to be detrimental for rabbits, since these are not optimum and, to a great extent this is owing to land-use changes during 453 399 habitats for the species (Lombardi et al. 2003). From this point the last century (Smith 2008). Although it has been previously 454 400 of view, the large decrease in dense scrubland in municipalities suggested that habitat loss and fragmentation has been a major 455 401 where rabbit favourability has decreased would be positive. cause of rabbit decline (Ward 2005), our study provides the 456 402 However, dense scrubland has apparently been replaced in first empirical evidence showing that habitat changes have 457 403 these areas by other habitats unfavourable to rabbits, such been highly detrimental for this keystone species in the Iberian 458 404 as herbaceous crops with oaks (Table 3). In fact, the area Mediterranean ecosystem. Following the rabbit population 459 405 devoted to herbaceous crops with oaks has tremendously decline, conservationists and hunters have applied a great 460 406 increased in those municipalities where rabbit favourability number of management tools to improve rabbit densities (for 461 407 has decreased (Table 3). Not only has the surface area of this example Delibes-Mateos et al. 2008b). Based on our findings, it 462 408 type of habitat (typically called dehesa) increased in the study is to be expected that these strategies would be unsuccessful in 463 409 area, but it has also undergone structural modifications. The areas where favourable habitats for rabbits have disappeared 464 410 scrub layer traditionally linked to the dehesa has progressively as a consequence of landscape changes. Thus, it would be 465 411 disappeared as a consequence of agriculture and livestock preferable to conserve and recover the landscapes suitable for 466 412 intensification (Fernandez-Al´ es´ et al. 1992). It is known that the species. 467 413 improvements associated with modern agricultural practices 414 can have long-term detrimental effects on rabbit populations 415 (Boag 1987). Interestingly, land uses suitable for rabbits in ACKNOWLEDGEMENTS 468 416 both models (Table 2) have increased in municipalities where 417 rabbit favourability has also increased (Table 3; see also M. Delibes-Mateos was supported by a postdoctoral grant 469 418 Fig. 4a). Therefore, an improvement in rabbit habitat has from the regional government of Castilla la Mancha (JCCM) 470 419 occurred in these locations. In addition, the reduction of the and the European Social Fund (ESF). Special thanks go to E. 471 420 surface area devoted to herbaceous crops with oaks and to Mart´ınez for providing the maps of the abundance of game 472 421 dense scrubland has contributed to the habitat improvement species during the 1960s. We are indebted to D. Anderson, 473 422 recorded in these areas. N. Fernandez,´ J. FernandezdeSim´ on,´ D. Parish and two 474 423 We have not addressed specifically the effect of diseases anonymous reviewers for helpful comments on previous drafts 475 424 on rabbit population decline. Nevertheless, a recent review of the manuscript. The Consejer´ıa de Medio Ambiente de 476 425 has showed that positive rabbit trends, after the initial RHD la Junta de Andaluc´ıa kindly supplied the Annual Hunting 477 426 outbreak, have been recorded in species-friendly habitats Reports. 478 427 (Delibes-Mateos et al. 2009b). Similarly, a theoretical model 428 also showed that the long-term impact of RHD is conditioned 429 by population dynamics, which are primarily determined by References 479 430 habitat suitability (Calvete 2006). According to these findings, Barcena,´ S., Real, R., Olivero, J. & Vargas, J.M. (2004) Latitudinal 480 431 the impoverishment of rabbit preferred habitat observed in trends in breeding waterbird species richness in and their 481 432 the present study could be jeopardizing rabbit recovery in the environmental correlates. Biodiversity and Conservation 13: 1997– 482 433 Iberian Peninsula. 2014. 483 Boag, B. (1987) Reduction in numbers of the wild rabbit (Oryctolagus 484 cuniculus) due to changes in agricultural practices and land use. 485 434 CONCLUSIONS Crop Protection 6: 347–351. 486 435 The availability of hunting records with explicit time and Borcard, D., Legendre, P. & Drapeau, P. (1992) Partialling out the 487 spatial component of ecological variation. Ecology 73: 1045–1055. 488 436 space references allows the development of datasets which Calvete, C. (2006) Modelling the effect of population dynamics on 489 437 can be used to analyse species trends in historic and regional the impact of rabbit hemorrhagic disease. Conservation Biology 20: 490 438 contexts (Fernandez´ & Ruiz de Azua 2009). We have used 1232–1241. 491 439 two sources based on hunting records, which were previously Calvete, C., Estrada, R., Angulo, E. & Cabezas-Ruiz, S. (2004) 492 440 used to assess changes in species abundance and distribution Habitat factors related to wild rabbit conservation in an agricultural 493 441 (Gortazar´ et al. 2000; Delibes-Mateos et al. 2009a), to estimate landscape. 19: 531–542. 494 442 long-term rabbit population trends. Our aim was to detect Calvete, C., Pelayo, E. & Sampietro, J. (2006) Habitat factors related 495 443 areas favourable to rabbits, thus to avoid potential bias owing to wild rabbit population trends after the initial impact of rabbit 496 444 to the existence of differences in the nature and quality of haemorrhagic disease. Wildlife Research 33: 467–474. 497 8 M. Delibes-Mateos et al.

498 Cartron, J.L.E., Kelly, J.F. & Brown, J.H. (2000) Constraints on Legendre, P. (1993) Spatial autocorrelation: trouble or new 552 499 patterns of covariation: a case study in strigid owls. Oikos 90: paradigm? Ecology 74: 1659–1673. 553 500 381–389. Legendre, P. & Legendre, L. (1998) Numerical Ecology. Second 554 501 Delibes-Mateos, M., Delibes, M., Ferreras, P. & Villafuerte, R. English Edition. Amsterdam, the Netherlands: Elsevier Science. 555 502 (2008a) Key role of European rabbits in the conservation of the Lombardi, L., Fernandez,´ N., Moreno, S. & Villafuerte, R. 556 503 western Mediterranean Basin Hotspot. Conservation Biology 22: (2003). Habitat-related differences in rabbit (Oryctolagus cuniculus) 557 504 1106–1117. abundance, distribution and activity. Journal of Mammalogy 84: 558 505 Delibes-Mateos, M., Farfan,´ M.A., Olivero, J., Marquez,´ 26–36. 559 506 A.L. & Vargas, J.M. (2009a) Long-term changes in game Ministerio de Agricultura (1968) Mapa Cinegetico´ Nacional. Madrid, 560 507 species over a long period of transformation in the Iberian Spain: Ministerio de Agricultura. 561 508 Mediterranean landscapes. Environmental Management 43: 1256– Moreno, S. & Villafuerte, R. (1995) Traditional management of 562 509 1268. scrubland for the conservation of rabbits Oryctolagus cuniculus 563 510 Delibes-Mateos, M., Ferreras, F. & Villafuerte, R. (2009b) and their predators in Donana˜ National Park, Spain. Biological 564 511 European rabbit population trends and associated factors: a Conservation 73: 81–85. 565 512 review of the situation in the Iberian Peninsula. Mammal Review Munoz,˜ A.R. & Real, R. (2006) Assessing the potential range 566 513 39: 124–40. expansion of the exotic monk parakeet in Spain. Diversity and 567 514 Delibes-Mateos, M., Ram´ırez, E., Ferreras, P. & Villafuerte, R. Distribution 12: 656–665. 568 515 (2008b) Translocations as a risk for the conservation of European Piorno, V. (2006) Gestion´ cinegetica´ y conservacion´ del conejo de 569 516 wild rabbit Oryctolagus cuniculus lineages. Oryx 42: 259–264. monte. Ph.D. thesis, Universidad de Vigo, Vigo, Spain. 570 517 Delibes-Mateos, M., Redpath, S.M., Angulo, E., Ferreras, P. & Real, R., Barbosa, A.M. & Vargas, J.M. (2006) Obtaining 571 518 Villafuerte, R. (2007) Rabbits as a keystone species in southern environmental favourability functions from logistic regression. 572 519 Europe. Biological Conservation 137: 149–156. Environmental and Ecological Statistics 13: 237–245. 573 520 Farfan,´ M.A., Guerrero, J.C., Real, R., Barbosa, A.M. & Vargas, Rojas, A.B., Cotilla, I., Real, R., Palomo, L.J. (2001) Determinacion´ 574 521 J.M. (2004) Caracterizacion´ del aprovechamiento cinegetico´ de de las areas´ probables de distribucion´ de los mam´ıferos terrestres 575 522 los mam´ıferos en Andaluc´ıa. Galemys 16: 41–59. en la provincia de Malaga´ a partir de las presencias conocidas. 576 523 Farfan,´ M.A., Vargas, J.M., Guerrero, J.C., Barbosa, A.M., Duarte, Galemys 13: 217–229. 577 524 J. & Real, R. (2008) Distribution modelling of wild rabbit hunting Smith, A.T. (2008) Conservation of endangered lagomorphs. In: 578 525 yields in its original area (S Iberian Peninsula). Italian Journal of Lagomorph Biology: Evolution, Ecology and Conservation, ed. P.C. 579 526 Zoology 75: 161–172. Alves & K. Hacklander,¨ pp. 297–315. Berlin, Germany: Springer- 580 527 Farr, T.G. & Kobrick, M. (2000) Shuttle Radar Topography Mission Verlag. 581 528 produces a wealth of data. EOS Transactions of the American US Geological Survey (1996) GTOPO30. Land Processes Distrib- 582 529 Geophysical Union 81: 583–585. uted Archive Center [www document].URL http://edcdaac.usgs. 583 530 Fernandez,´ J.M. & Ruiz de Azua, N. (2009) Historical dynamics gov/gtopo30/gtopo30.asp 584 531 of a declining wolf population: persecution vs. prey reduction. Vargas, J.M., Farfan,´ M.A., Guerrero, J.C., Barbosa, A.M. & Real, 585 532 European Journal of Wildlife Research (in press). R. (2007) Geographical and environmental correlates of big and 586 533 Fernandez,´ N. (2005) Spatial patterns in European rabbit abundance small game in Andalusia (southern Spain). Wildlife Research 34: 587 534 after a population collapse. Landscape Ecology 20: 897–910. 498–506. 588 535 Fernandez-Al´ es,´ R., Mart´ın, A., Ortega, F. & Ales, E.E. (1992) Vargas, J.M., Guerrero, J.C., Farfan,´ M.A., Barbosa, A.M. & Real, 589 536 Recent changes in landscape structure and function in a R. (2006) Land use and environmental factors affecting red- 590 537 Mediterranean region of SW of Spain (1950–1984). Landscape legged partridge (Alectoris rufa) hunting yields in Southern Spain. 591 538 Ecology 7: 3–18. European Journal of Wildlife Research 52: 188–195. 592 539 Galvez-Bravo,´ L., Belliure, J. & Rebollo, S. (2009) European Villafuerte, R., Vinuela,˜ J. & Blanco, J.C. (1998) Extensive predator 593 540 rabbits as ecosystem engineers: warrens increase lizard density persecution caused by population crash in a game species: the 594 541 and diversity. Biodiversity and Conservation 18: 869–885. case of red kites and rabbits in Spain. Biological Conservation 84: 595 542 Gortazar,´ C., Herrero, J., Villafuerte, R. & Marco, J. (2000) Historical 181–188. 596 543 examination of the status of large mammals in Aragon, Spain. Virgos,´ E., Cabezas-D´ıaz, S. & Lozano, J. (2007) Is the wild 597 544 Mammalia 64: 411–422. rabbit (Oryctolagus cuniculus) a threatened species in Spain? 598 545 Hosmer, D.W. & Lemeshow, S. (1989) Applied Logistic Regression. Sociological constraints in the conservation of species. Biodiversity 599 546 New York, NY, USA: John Wiley & Sons, Inc. and Conservation 16: 3489–3504. 600 547 Junta de Andaluc´ıa (1956) Mapa de usos y coberturas vegetales del suelo Ward, D. (2005) Reversing rabbit decline: one of the biggest 601 548 de Andaluc´ıa 1956. Sevilla, Spain: Consejer´ıa de Medio Ambiente. challenges for nature conservation in Spain and Portugal. 602 549 Junta de Andaluc´ıa (1999) Mapa de usos y coberturas vegetales del Technical report. World Conservation Union, Gland, Switzerland 603 550 suelo de Andaluc´ıa 1999. Sevilla, Spain: Consejer´ıa de Medio [www document]. URL http://www.ualberta.ca/∼dhik/lgs/ 604 551 Ambiente. report_lynx_rabit.pdf 605