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Key Role of European Rabbits in the Conservation of the Western Mediterranean Basin Hotspot MIGUEL DELIBES-MATEOS,∗ †§ MIGUEL DELIBES,‡ PABLO FERRERAS,∗ AND RAFAEL VILLAFUERTE∗ ∗ Instituto de Investigación en Recursos Cinegéticos, IREC (CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13071-Ciudad Real, Spain †Departamento de Biologı́a Animal, Facultad de Ciencias, Universidad de Málaga, 29071-Málaga, Spain ‡CSIC, Department of Applied Biology, Estac Biol Donana, ES-41013 Seville, Spain Abstract: The Mediterranean Basin is a global hotspot of biodiversity. Hotspots are said to be experiencing a major loss of habitat, but an added risk could be the decline of some species having a special role in ecological relationships of the system. We reviewed the role of European rabbits (Oryctolagus cuniculus) as a keystone species in the Iberian Peninsula portion of the Mediterranean hotspot. Rabbits conspicuously alter plant species composition and vegetation structure through grazing and seed dispersal, which creates open areas and preserves plant species diversity. Moreover, rabbit latrines have a demonstrable effect on soil fertility and plant growth and provide new feeding resources for many invertebrate species. Rabbit burrows provide nest sites and shelter for vertebrates and invertebrates. In addition, rabbits serve as prey for a number of predators, including the critically endangered Iberian lynx (Lynx pardinus) and Spanish Imperial Eagle (Aquila adalberti). Thus, the Mediterranean ecosystem of the Iberian Peninsula should be termed “the rabbit’s ecosystem.” To our knowledge, this is the first empirical support for existence of a multifunctional keystone species in a global hotspot of biodiversity. Rabbit populations have declined drastically on the Iberian Peninsula, with potential cascading effects and serious ecological and economic consequences. From this perspective, rabbit recovery is one of the biggest challenges for conservation of the Mediterranean Basin hotspot. Keywords: biodiversity hotspot, ecosystem engineer, European rabbit, hotspot conservation, keystone species, Mediterranean ecosystem, Oryctolagus cuniculus Papel Clave de Conejos Europeos en la Conservación del Área de Importancia del Mediterráneo Occidental Resumen: La Cuenca del Mediterráneo es un área de importancia para la biodiversidad global. estas áreas de importancia están experimentando una gran pérdida de hábitat, pero el declive de algunas especies que juegan un papel especial en las relaciones ecológicas del sistema pudiera ser un riesgo adicional. Revisamos el papel del conejo europeo (Oryctolagus cuniculus) como especie clave en la porción del área de importancia Mediterráneo en la Penı́nsula Ibérica. Los conejos conspicuamente alteran la composición de especies de plantas y la estructura de la vegetación por medio del pastoreo y la dispersión de semillas, lo cual crea áreas abiertas y preserva la diversidad especies de plantas. Más aun, las letrinas de conejos tienen un efecto demostrable sobre la fertilidad del suelo y el crecimiento de plantas y proporcionan nuevos recursos alimenticios para muchas especies de invertebrados. Las madrigueras de los conejos proporcionan espacio para la nidificación y refugio a vertebrados e invertebrados. También, los conejos sirven como presa para un nú mero de depredadores, incluyendo al lince ibérico (Lynx pardinus) en peligro crı́tico y al águila imperial (Aquila adalberti). Por lo tanto, el ecosistema Mediterráneo de la Penı́nsula Ibérica deberı́a ser denominado el “ecosistema de los conejos.” Hasta donde sabemos, este es la primera evidencia empı́rica de la existencia de una especie clave multifuncional en un área de importancia para la biodiversidad global. Las poblaciones §Address for correspondence: Departamento de Biologı́a Animal, Facultad de Ciencias, Universidad de Málaga, 29071- Málaga, Spain, email [email protected] de conejos han declinado drásticamente en la Penı́nsula Ibérica, con potenciales efectos en cascada y serias consecuencias ecológicas y económicas. Desde esta perspectiva, la recuperación de conejos es uno de los mayores retos para la conservación del área de importancia de la Cuenca del Mediterráneo. Palabras Clave: área de importancia para la biodiversidad, conservación de área de importancia, ecosistema del Mediterráneo, especies clave, ingeniero de ecosistemas, Oryctolagus cuniculus Introduction As many as 34 global biodiversity hotspots, described as “areas featuring exceptional concentrations of endemic species and experiencing exceptional loss of habitat,” have been identified (Myers et al. 2000; Mittermeier et al. 2005). A usually overlooked risk for hotspots is the decline or disappearance of some key species, which could produce catastrophic cascading effects on the whole system (Chapin et al. 2000). We reviewed the key role of European rabbits (Oryctolagus cuniculus) at the western corner of the Mediterranean Basin hotspot. Rabbit populations are currently declining in this area (Ward 2005), which should be a cause for concern in conservation of the composition, functions, and processes of this hotspot. Mediterranean-type ecosystems occur in rather small areas in America (California and Chile), South Africa, Australia, and around the Mediterranean Sea (Di Castri & Mooney 1973). These areas, characterized by hot, dry summers and mild, rainy winters, are centers of biodiversity, second only to the tropics in importance (Cowling et al. 1996). The Mediterranean Basin hotspot includes the Iberian Peninsula, which was a refuge for temperate species during past glaciations (Taberlet et al. 1998). Its high mountains (e.g., Sierra Nevada, southern Spain, approximately 3500 m asl) are a southern refuge for northern ecotypes. Consequently, a large number of endemic species occur in Mediterranean Iberia (e.g., over 1500 endemic species in the Spanish flora; MMA 2008). Iberian Mediterranean natural habitats have been lost to, for example, cultivation, tree plantations, reservoirs, and urbanization (e.g., Symeonakis et al. 2007). Nevertheless, an additional risk could be the decline of the European rabbit, which is endemic to the Iberian Peninsula (Monnerot et al. 1994). From the late Pleistocene until Classical antiquity, European rabbits were present only on the Iberian Peninsula and in a small area in southern France (Monnerot et al. 1994). The species is now distributed widely in Europe, South America, Australia, and many oceanic islands (Gibb 1990) as a consequence of human introductions. European rabbits are opportunistic and highly adaptable, which explains their success as colonists (Gibb 1990). Because of their wide distribution and their potentially high population densities, rabbits have pronounced effects on biological diversity and ecosystem functions. Where introduced, they can destroy vegetation, damage farm crops, compete with livestock and native wild species, and cause severe ecological damage (Thompson & King 1994). Consequently, numerous attempts have been made to eradicate introduced rabbits, including the artificial spread of exotic disease agents (Angulo & Cooke 2002). In spite of recent population declines (see later), rabbits still can reach high abundances in some of their natural Mediterranean habitats, where their ecological effects are evident (Ward 2005). Nevertheless, because they evolved in this area, they are central to processes that maintain integrity of biodiversity in the region. We reviewed the role of rabbits as ecosystem engineers, with specific focus on their effects on vegetation structure and composition, through herbivory and seed dispersal; the importance of their latrines for soil condition and for invertebrates; and their effects as diggers, providing a refuge for a variety of animal species. We also considered the role of rabbits as prey for many Iberian predators. We discuss current trends in rabbit abundance and the potential implications of these trends for the conservation of biodiversity in the western corner of Mediterranean Basin hotspot. Because most of the studies we reviewed were conducted in recent decades, after the rabbit decline began on the Iberian Peninsula, we focused primarily on qualitative rather than quantitative aspects of their role in the ecosystem. Nevertheless, it is likely that their effects on the ecosystem were greater before their decline than they are now. Because there is little scientific information on rabbit populations in this area beyond 30 years ago, we occasionally drew on information from other regions. The Rabbit as an Ecosystem Engineer Abiotic environmental conditions and species interactions have been proposed as determinants of species diversity patterns in natural communities (Tilman 1999). Even though all species interact with their physical environment, some organisms substantially influence environmental conditions and resource availability and thus affect other species and the community attributes of natural species assemblages. Jones et al. (1994) coined the Conservation Biology Volume 22, No. 5, 2008 Figure 1. Dominant pathways by which European rabbits affect ecosystem structure and function in the Mediterranean area of the Iberian Peninsula (inspired by Kotliar et al. 1999). phrase physical ecosystem engineering for this biotic process and physical ecosystem engineers to refer to the organisms responsible for such habitat changes. Rabbits are special among leporids because they form colonies, reach high densities, and dig warrens (Gibb 1990). The primary rabbit activities that have ecosystemlevel consequences are herbivory, seed dispersal, digging (warren building and scratching), and depositing feces, mainly at latrines (Fig. 1). Rabbit Grazing and Plant Species Diversity Many researchers have noted the effects of rabbit grazing on the composition and structure of plant communities (e.g., Watt 1981; Eldridge & Simpson 2002). Although most of these studies concern areas where rabbits are considered a pest, a number have been made in the Iberian ecosystem. Soriguer (1981) estimated that rabbits consume approximately 15% of the available vegetation biomass in Doñana National Park, southwestern Spain. In a recent study in central Spain, Rueda (2006) observed that rabbits eat 42% of the total aboveground biomass, equivalent to 80% of the biomass consumed by all vertebrate herbivores in this area. Where rabbits are numerous (>40 individuals/ha have been recorded in some areas, in Conservation Biology Volume 22, No. 5, 2008 spite of diseases; Palomares 2001), they have substantial effects on the aboveground flow of energy and materials. Consequently, excluding rabbit grazing from a plant community causes marked changes in community composition (Garcı́a-Fuentes et al. 2006; Rueda 2006). Rabbits exhibit high grazing selectivity in areas where they have been introduced (Leigh et al. 1989); hence, palatable or preferred plants are less abundant where rabbits reach high numbers (Eldridge & Simpson 2002). In southern Spain, the abundance of palatable plants (mainly Poaceae and Fabaceae species) decreases in rabbit-grazed grasslands, whereas that of less-preferred species (mainly Asteraceae species) increases (Garcı́aFuentes et al. 2006). Some plant species may increase in abundance where rabbits are grazing because of reduced interspecific competition (Crawley 1990). In addition, continuous rabbit grazing reduces mean plant size and increases size inequality (Crawley & Weiner 1991), although the largest plants can occur in grazed areas due to reduction in competition (Eldridge & Simpson 2002). Herbivory by rabbits influences spatial patterns of dominant woody species in the Mediterranean landscape. Gómez-Sal et al. (1999) demonstrated that disturbance by rabbits produces Retama sphaerocarpa patches with fewer, more scattered, thicker-branched, and larger shrubs (i.e., an open scrubland or savannahtype structure). Thus, rabbits promote the maintenance of open scrubland, which is their preferred habitat (Moreno & Villafuerte 1995). In contrast, anthropogenic disturbances, such as mechanical cutting or fires, tend to produce denser shrubs with a greater canopy biomass (Gómez-Sal et al. 1999), which is unsuitable as rabbit habitat. The activity of rabbits in creating mosaics of open areas and promoting growth of an herbaceous layer in scrubland (Gómez-Sal et al. 1999; see also Oosterveld 1983) may facilitate settlement of other herbivores that depend on this type of habitat. Grazing by rabbits and brown hares (Lepus europaeus) in some regions of the Netherlands prevents tall plant species from becoming dominant, which enhances feeding conditions for Brent Geese (Branta bernicla) (van der Wal et al. 2000). On the Iberian Peninsula, where the small mammal community is richer than in other Mediterranean areas (Cagnin et al. 1998), rabbit grazing may favor several species of small mammals because their preferred habitat, ecotones between cover and open areas (e.g., Hansson 1998), is promoted by rabbit grazing. Moreover, the predation risk for small mammals may be higher in open areas, such as those created by rabbits. Thus, predators associated with open areas would benefit indirectly from rabbit grazing. Therefore, rabbits tend to increase habitat complexity and heterogeneity, causing species abundances and/or richness to rise. Endozoochorous Seed Dispersal by Rabbits In recent decades a considerable body of knowledge has accumulated regarding the role of frugivores as seed dispersers in the Mediterranean region (Jordano & Schubb 2000). Rabbits damage some kinds of seeds in their gastrointestinal tract (J. M. Fedriani, personal communication), but their dung can contain viable seeds from a large range of herbaceous, shrub, and tree species. In the Mediterranean region, these include at least 72 plant species belonging to 23 different families (Table 1). In some instances, seed germination rate and success are higher in seeds in rabbit dung (Cerván Carmona & Pardo Navarro 1997; Dellafiore et al. 2006). Typically a small proportion of rabbit pellets contain seeds (approximately 2.5%; Malo et al. 2000; Dellafiore et al. 2006). Nevertheless, the number of seeds dispersed by rabbits during the year is large because there are usually several individuals per hectare and each individual produces approximately 325 pellets per day (Wood 1988). Rabbits are thus very important seed vectors, contributing to plant population recruitment and facilitating long-distance dispersal of seeds into habitats not previously colonized (Dellafiore et al. 2006). Rabbits eat the fruiting bodies of fungi (Alves et al. 2006), and they likely disperse fungal spores that de- velop mycorrhizal associations, contributing to the development of vegetation, as occurs in other small mammals (Dickman 1999; Johnson 1996). To our knowledge this important topic has not been addressed. Rabbit Latrines, Soil Nutrients, and Dung Beetle Diversity As well as scattering fecal pellets, rabbits deposit a large number of pellets (sometimes >1000) that serve a social function in latrines. Latrines can be used for a number of years (Gibb 1993). Although the use of latrines varies among rabbit populations, latrine use is usually high when rabbits are abundant. Densities of almost 80 and 110 latrines/ha have been reported from central Spain (Gálvez et al. 2008) and southern Spain (Petterson 2001), respectively. Dung deposition by stock animals creates localized patches of high nutrient concentrations that affect the sward and soil microbial activity (Lovell & Jarvis 1996). Rabbit fecal pellets have total N and P concentrations comparable to the dung of stock animals; hence, latrines have a demonstrable effect on soil fertility and plant growth, creating fertile islands between shrubs (Willot et al. 2000). In southern Spain rabbit latrines alter composition, density, and biomass of the surrounding vegetation (e.g., a 3-fold increase of biomass and 16% less bare ground; Petterson 2001). Therefore, by importing nutrients to latrines, rabbits create heterogeneity and increase diversity in the semiarid Mediterranean ecosystem (Petterson 2001). Rabbit latrines also provide new feeding resources for many invertebrate species. For instance, Mediterranean dung beetles, including Onthophagus latigena and O. emarginatus, are frequently collected from rabbit pellets (Sánchez-Piñero & Ávila 1991; Galante & Cartagena 1999). The availability and abundance of dry pellets (especially from rabbits) seem to be key factors in the evolutionary diversification and high level of endemism in Mediterranean dung beetles (Verdú & Galante 2002). Some species associated with rabbit pellets show anatomical adaptations of their mouth parts (e.g., prominent denticles and well-developed molar areas) that apparently favor exploitation of dry fibrous dung, such as rabbit pellets (Verdú & Galante 2004). Rabbit Warrens and Surface Digging As their scientific name implies (oryktes means digger in Greek), rabbits are burrowing animals that live communally in warrens (Gibb 1990). The importance of warrens to rabbits has been highlighted by many authors (Kolb 1991; Palomares 2003), and large, healthy rabbit populations are usually associated with high warren densities (Blanco & Villafuerte 1993). Warren densities vary greatly. The highest density reported to date was 496 burrow entrances/ha in Britain (Kolb 1991). In southwestern Spain, Palomares (2001) estimated a total of Conservation Biology Volume 22, No. 5, 2008 Table 1. Plant species reported to be dispersed by European rabbits in the Iberian Peninsula. Plant species Andryala integrifolia Apera interrupta Aphanes microcarpa Arabidopsis thaliana Arenaria leptoclados Armeria gaditana Asparagus aphyllus Asphodelus aestivus Biserrula pelecinus Brassica barrelieri Campanula erinus Capsella bursa-pastoris Cerastium glomeratum C. semidecandrum Cistus ladanifer Cis. salvifolius Crassula tillaea Corema album Crepis capillaris Cruciata pedemontana Erophila verna Filago pyramidata Galium murale G. parisiense G. spurium Halimium halimifolium Heliotropium europaeum Herniaria hirsuta Juncus bufonius J. inflexus Juniperus macrocarpa Jun. phoenicea Lavandula stoechas Legousia castellana Logfia minima Lophocloa cristata Myosotis persoonii Myo. stricta Olea europaea Parentucellia latifolia Phillyrea angustifolia Pistacia lentiscus P. terebinthus Plantago afra Pla. coronopus Pla. loeflingii Poa annua Po. bulbosa Polycarpon tetraphyllum Polypogon monspeliensis Retama monosperma R. sphaerocarpa Rosmarinus officinalis Sagina apelata Sisymbrium runcicatum Spergularia purpurea Stellaria media Trifolium campestre T. cernuum T. glomeratum T. retusum T. suffocatum Family References Asteraceae Poaceae Rosaceae Brassicaceae Caryophyllaceae Plumbaginaceae Liliaceae Liliaceae Leguminosae Brassicaceae Campanulaceae Brassicaceae Caryophyllaceae Caryophyllaceae Cistaceae Cistaceae Crassulaceae Empetraceae Asteraceae Rubiaceae Brassciaceae Asteraceae Rubiaceae Rubiaceae Rubiaceae Cistaceae Boraginaceae Caryophyllaceae Juncaceae Juncaceae Cupressaceae Cupressaceae Lamieaceae Campanulaceae Asteraceae Poaceae Boraginaceae Boraginaceae Oleaceae Scrophulariaceae Oleaceae Anacardiaceae Anacardiaceae Plantaginaceae Plantaginaceae Plantaginaceae Poaceae Poaceae Caryophyllaceae Poaceae Leguminosae Leguminosae Lamieaceae Caryophyllaceae Brassicaceae Caryophyllaceae Caryophyllaceae Leguminosae Leguminosae Leguminosae Leguminosae Leguminosae Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Rogers et al. 1994 Rogers et al. 1994 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Soriguer 1986; Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Rogers et al. 1994; Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Soriguer 1986 Muñoz Reinoso 1993; Rogers et al. 1994 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Soriguer 1986; Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Rogers et al. 1994 Rogers et al. 1994 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Dellafiore et al. 2006 Rogers et al. 1994; Cerván Carmona & Pardo Navarro 1997 Rogers et al. 1994 Malo & Suárez 1995; Malo et al. 1995; 2000 Malo & Suárez 1995; Malo et al. 1995; 2000 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 Malo et al. 1995 Malo & Suárez 1995; Malo et al. 1995 continued Conservation Biology Volume 22, No. 5, 2008 Table 1. (continued) Plant species T. tomentosum Tuberaria guttata Urtica urens Veronica arvensis V. verna Viola kitaibeliana Vulpia bromoides Vul. ciliata Vul. muralis Vul. unilateralis Family Leguminosae Cistaceae Urticaceae Scrophulariaceae Scrophulariaceae Violaceae Poaceae Poaceae Poaceae Poaceae 266 warren entrances/ha (7 warrens/ha) and an average of 38.1 entrances/warren in areas of Mediterranean scrubland within Doñana National Park. Thus, rabbit warrens are important components of the Mediterranean landscape. Garcı́a y Bellido (1945) quoted classic Greek and Roman authors who recorded that the burrowing activity of rabbits in ancient times was sufficient to undermine the buildings of entire cities in the Baleares Islands. Rabbit warrens provide new feeding and refuge areas for many other species (Gálvez et al. 2008). For instance, rabbits in Spain support at least 22 genera of ectoparasites (compared with 8 in Australia, 7 of which also have been recorded in Spain; Soriguer 1980). Among these are several species of rabbit flea (Spilopsyllus cuniculi, Xenopsylla cunicularis, Echidnophaga iberica, Caenopsylla laptevi, Odontopsyllus quirosi) that can be found in high numbers in rabbit warrens (Rogers et al. 1994) and can act as important disease vectors for rabbits and other species (Osácar-Jiménez et al. 2001). Amphibians, reptiles, mammals, and some birds frequently use rabbit warrens. The common toad (Bufo bufo), the natterjack toad (B. calamita), the common midwife toad (Alytes obstetricans), and the newt (Pleurodeles waltl) occur in rabbit warrens (authors’ unpublished data). Blázquez and Villafuerte (1990) observed the Montpellier snake (Malpolon monspessulanus) nesting inside rabbit warrens, and other snakes and some lizard species (Gálvez 2008) also inhabit rabbit warrens. Among small mammals, the garden dormouse (Eliomys quercinus), wood mouse (Apodemus sylvaticus), Algerian mouse (Mus spretus), and 2 species of rat (Rattus norvegicus, R. rattus) have been found inside rabbit warrens (authors’ unpublished data). Several species of carnivores use rabbit burrows as refuges. For instance, Eurasian badgers (Meles meles) commonly construct diurnal resting dens by enlarging existing rabbit warrens (Revilla et al. 2001). Other carnivores, such as the polecat (Mustela putorius), Egyptian mongoose (Herpestes ichneumon), red fox (Vulpes vulpes), and weasel (M. nivalis), also use rabbit warrens as resting sites (Blas-Aritio 1970; Palomares & Delibes 1993; C. Rouco, personal communication). Female Iberian lynx (Lynx pardinus) References Malo & Malo & Malo & Malo & Malo & Malo & Malo & Malo & Malo & Malo & Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 Suárez 1995; Malo et al. 1995 and wolves (Canis lupus) use enlarged rabbit warrens as temporary shelter for their young (authors’ unpublished data). Some birds, such as the Little Owl (Athene noctua), use rabbit warrens as nesting places (authors’ unpublished data). Like other species of small mammals (Dickman 1999), rabbits may also affect nutrient cycling, water flow, soil structure, and microtopography with their continuous and intensive digging (warren building and scratching). Rabbits as Prey for Humans and Other Animals Small mammals such as rabbits were a major component of the diet of Iberian people from the Palaeolithic to the Bronze Age (e.g., Callou 2003). The use of wild rabbits decreased after the species was domesticated, but wild rabbit meat was valuable even during the first decades of the 20th century (Delibes 1972). Today, rabbit hunting is an economically important sport on the Iberian Peninsula. In Spain over 30,000 private hunting estates cover over 70% of the country (Angulo & Villafuerte 2003), more than 1 million people hunt every year, and many of these people preferentially hunt rabbits (Rogers et al. 1994). Despite the recent history of dramatic decreases or even localized extinction of many rabbit populations (Villafuerte et al. 1995), rabbits are still the most-hunted species in Spain in both number and biomass (>4 million rabbits are currently harvested annually; INE 2006; Fig. 2). Rabbits are also an important prey species for many wild predators in the Iberian Mediterranean ecosystem (Table 2; see also Valverde 1967; Ward 2005). In Spain, for example, rabbits are important prey for more than 30 nocturnal and diurnal predators (Delibes & Hiraldo 1981). Large predators tend to consume more rabbits and, with the exception of the wolf, all predators of medium and large size (>3 kg among the mammals and >1.5 kg among the birds) feed primarily on rabbits when they occur at high density, whereas nearly all smaller predators use rabbits as alternative prey (Delibes & Hiraldo 1981; Jaksic & Delibes 1987). Conservation Biology Volume 22, No. 5, 2008 Oryctolagus cuniculus Alectoris rufa Lepus spp Sus scrofa Cervus elaphus 0 1 2 3 4 5 Individuals hunted (millions) Figure 2. Number of individuals of the primary game species taken by hunters in Spain during the 2001 hunting season (INE 2006). Two flagship species of conservation concern in Europe, the Spanish Imperial Eagle (Aquila adalberti) and the Iberian lynx, both endemic to the Iberian Mediterranean ecosystem, probably evolved as “super specialists” on rabbits. Rabbits constitute over 85% of the diet of the Iberian lynx (Table 2). Moreover, rabbit densities of at least 1–4.6 rabbits/ha (during autumn and spring, respectively) are necessary to sustain territorial breeding lynx (Palomares et al. 2001). The proportion of rabbits in the diet of Spanish Imperial Eagles is rather low (Table 2), but a recent study demonstrated that eagle distribution is strongly correlated with areas of high rabbit density (Delibes-Mateos et al. 2007). That Spanish Imperial Eagle and the Iberian lynx preyed on rabbits in the Pleistocene refugium of southern Spain may have played an essential role in the phylogenetic segregation of these species from their sister species, the Eastern Imperial Eagle (A. heliaca) and the Eurasian lynx (L. lynx), respectively (Ferrer & Negro 2004). Several Mediterranean species are facultative rabbit predators, specializing locally on rabbits where they are abundant. At high densities rabbits are ideal prey because of their high energetic value and low catchability costs (Revilla & Palomares 2002; Malo et al. 2004). Facultative predators include carnivores and birds of prey, some of them of international conservation concern, such as the Bonelli’s Eagle (Hieraaetus fasciatus; Table 2). Many other predator species feed opportunistically on rabbits. For instance, the high availability of young and juvenile rabbits in spring provides an important food resource for several small birds of prey and generalist carnivores. Viñuela and Veiga (1992) observed a positive relationship between the breeding success of the Black Kite (Milvus migrans) and the proportion of its diet consisting of juveniles or sick rabbits. Some scavengers of international conservation concern, such as the Black Vulture Conservation Biology Volume 22, No. 5, 2008 (Aegypius monachus) (Hiraldo 1976), consume rabbit carcasses and kill juvenile rabbits in areas where rabbit density is high. The rare Bearded Vulture (Gypaetus barbatus) consumes rabbits in the Pyrenees (Margalida et al. 2005). Rabbits were probably an important resource for this species before it disappeared from southern Spain (Hiraldo et al. 1979). Other species feed occasionally on rabbits, but they represent a small proportion of their diet even when rabbit densities are high (Table 2). According to Valverde (1967), big Montpellier snakes became scarce in Doñana National Park after introduction of myxomatosis in the 1950s and subsequent decline of rabbits (the snakes’ main prey). The only estimate of the absolute number of rabbits consumed by the entire predator community in Mediterranean Spain was made by Kufner (1986) for Doñana Biological Reserve, southwestern Spain, before arrival of the rabbit hemorrhagic disease (RHD). She suggests that predators consumed about 51,000 rabbits annually in the 6,000-ha reserve, equivalent to more than 8 rabbits/ha. Rabbits constitute an important food source for many predators in the Mediterranean ecosystem. It is not surprising that the abundance of raptor species (species that take rabbits or scavenge on rabbit carcasses) is highly correlated with rabbit abundance in southern Spain (DelibesMateos et al. 2007). Consequently, rabbit abundance may allow pinpointing areas of current or future concern for conservation of predator species that are rare at the global or European scale. Rabbit Decline and Its Implications for Conservation Mediterranean-type ecosystems are good models for studying the impacts of global change and the 1113 Delibes-Mateos et al. Table 2. Contribution of rabbits to the diet of the main Iberian predators.a Main rabbit predators Carnivores Canis lupus Felis silvestris Genetta genetta Herpestes ichneumon Lynx pardinus Martes foina Meles meles Mustela putorius Vulpes vulpes Birds of prey Accipiter gentilis Aegypius monachus Aquila chrysaetos A. adalberti Bubo bubo Buteo buteo Circus aeruginosus Cir. cyaneus Cir. pygargus Hieraaetus fasciatus H. pennatus Milvus migrans Mil. milvus Neophron percnopterus Strix aluco Other predators birds: Accipiter nisus, Athene noctua, Ciconia ciconia, Circaetus gallicus, Corvus corax, Elanus caeruleus, Falco columbarius, F. peregrinus, F. subbuteo, F. tinnunculus, Grus grus, Gypaetus barbatus, Gyps fulvus, Larus argentatus, Tyto alba; mammals: Erinaceus algirus, E. europaeus, Mustela nivalis, Sus scrofa; reptiles: Elaphe scalaris, Lacerta lepida, Malpolon monpessulanus Type of rabbit predator Rabbit in diet (%) (min-max)b IUCN statusc opportunist facultative opportunist facultative specialist opportunist facultative opportunist facultative 0–44.4 0–64 2.8–11.4 22.2–80.3 77.5–99.5 0–20.4 0.01–61.8 0–30 0–96.1 NT VU LC DD CE LC LC NT LC opportunist facultative facultative specialist facultative opportunist opportunist opportunist opportunist facultative opportunist opportunist opportunist opportunist opportunist 12–22.4 23.9–70.7 13–63.2 27.4–55.8 16.9–67.5 0–66.6 0–22.8 0–31.9 1–17.2 12.6–51 2–60 1.6–56.7 8.3–29.2 2.5–49.3 8–38.27 LC VU NT EN LC LC LC LC VU EN LC NT EN EN LC occasional 0–<5 — a Data from Delibes and Hiraldo (1981), Valkama et al. (2005), and Moleón (2007). of occurrence (gut contents or scats) for carnivores and percentage of total prey remains for birds of prey. c Category definitions: CE, critically endangered; DD, data deficient; EN, endangered; LC, least concern; NT, near threatened; VU, vulnerable. b Percentage relationship between biological diversity and ecological function (Lavorel et al. 1998). Introduced species, including microorganisms, are an important component of human-induced change (Vitousek et al. 1997). Species introductions risk modifying the functioning of the Iberian Mediterranean ecosystem through their effects on rabbit populations because 2 exotic viral diseases, myxomatosis in the 1950s and RHD at the end of the 1980s, are the main causes of a sharp decline in rabbits in recent decades (Muñoz 1960; Villafuerte et al. 1995). Both diseases were introduced as biological control agents in areas where rabbits are considered a pest (Angulo & Cooke 2002). The rabbit population in Spain declined by an estimated 70% between 1973 and 1993 (Virgós et al. 2007). An even greater decline, perhaps over 90%, may have occurred because of myxomatosis in the 1950s; this disease has killed 90–100% of all rabbits in other regions (e.g., Armour & Thompson 1955). The decline of rabbits in the Iberian Peninsula has been almost general, but recovery has been spatially uneven. In many areas rabbits are extinct or survive at low densities, but in other areas their numbers are high enough to allow hunting. The recovery seems to have been greater in hunting areas (Delibes-Mateos et al. 2008a); hence, rabbit densities are currently lower in protected areas, perhaps because of different management practices and predation pressures (Delibes-Mateos 2006). Nevertheless, local and regional declines have been so acute in some parts of the Iberian Peninsula that rabbits have been recently classified as near threatened by the Portuguese Institute for Nature Conservation (Cabral et al. 2005) and as vulnerable on the Spanish Red List (Villafuerte & Delibes-Mateos 2007). Ecosystem processes can exhibit abrupt thresholds owing to the severe decline of a key species (Chapin et al. 2000). The decline in rabbit numbers could have important cascading effects on functioning of the Iberian Conservation Biology Volume 22, No. 5, 2008 1114 Mediterranean ecosystem and serious ecological and economic consequences. Some of these effects are becoming evident. For instance, considerable effort and funds are being expended to reestablish rabbit populations for sport hunting and to provide resources for predators through measures such as vaccination against diseases and restocking programs (Calvete et al. 1997; Moreno et al. 2004). Although 2 genetic lineages of rabbits are recognized, restocking practices frequently ignore this, risking conservation of genetic diversity (Delibes-Mateos et al. 2008b). Management actions are often not successful because the decline of rabbit numbers makes an area less suitable for subsequent recolonization (rabbits engineer the habitat to their own benefit by, for instance, opening it up and promoting the growth of an herbaceous layer). Opening the scrubland may have important indirect effects, such as reducing the amount of available combustible material and thus reducing the risk of catastrophic field fires (e.g., Piñol et al. 1998). It is widely accepted that the dramatic decrease in rabbit numbers has affected the reproductive success of some predators (Fernández 1993; Real & Mañosa 1997). Moreover, declines in the Iberian lynx and the Spanish Imperial Eagle seem to be at least partially due to reductions in rabbit abundance (Moreno et al. 2004). The rabbit decline must be affecting many other aspects of the Iberian Mediterranean ecosystem, including availability of refuges (for invertebrates, lizards, amphibians, and mammals), nutrient cycling, diversity of plant species, and abundance of specialist rabbit-pellet dung beetles. Evidence of the consequences for other communities and ecological processes caused by rabbit decline is currently lacking because there have been no long-term studies in the Mediterranean ecosystem. Nevertheless, a wide variety of studies conducted in other areas indicate that rabbit decline does affect other communities (e.g., plant and invertebrate communities) and ecological processes (Priddel et al. 2000 and references therein). Perhaps many Mediterranean species and processes have already been affected by the recent decline in rabbit abundance on the Iberian Peninsula. Conclusions: the Rabbit’s Ecosystem According to Power et al. (1996), a keystone species should have disproportionately large effects relative to its abundance, which seems to exclude abundant species, such as the European rabbit. Nevertheless, Kotliar (2000) proposed that species performing roles not performed by other species and processes should also be considered keystone species regardless of their abundance. Undoubtedly, rabbits fit this definition because they are crucial for maintaining the organization, functioning, and diversity of the ecological community. Mills et al. (1993) classified 5 functional types of keystone species: predators, Conservation Biology Volume 22, No. 5, 2008 Rabbits and the Mediterranean Basin prey, hosts, mutualists, and habitat modifiers. Rabbits fulfill almost all these functions in the Iberian Mediterranean ecosystem (Fig. 1). The role of rabbits as an important prey species in Mediterranean Iberia has been debated previously, but this is the first review of the different key roles that rabbits play in this global biodiversity hotspot. Rabbits are so important in the Mediterranean scrubland of southwestern Europe that this ecosystem could be considered “the rabbit’s ecosystem.” The contribution of other small mammals to ecosystem diversity and function has been shown previously (e.g., many rodents; Dickman 1999). Some species of small mammals are also keystone species because of their abundance and ecological importance. The role of rabbits in the Mediterranean ecosystem closely resembles that of the plateau pika (Ochotona curzoniae), a keystone lagomorph of the Tibetan plateau (Smith & Foggin 1999). The pika makes burrows that are the primary home to a variety of species, creates microhabitat disturbance, serves as the principal prey for several predators, and contributes positively to ecosystem-level dynamics. The role of rabbits in southern Europe is akin to the functional role of prairie dogs (Cynomys spp.) in prairie ecosystems of the United States because both are social-burrower species and can occur at high densities (Kotliar et al. 1999; Kotliar 2000). To our knowledge we present the first empirical evidence for the existence of a multifunctional keystone species in 1 of the 34 identified biodiversity hotspots. By definition, keystone species have a disproportionately large influence and their elimination or a large decline in numbers typically has a major effect on populations of other species and ecosystem processes (Chapin et al. 2000). Mediterranean scrubland biota in Spain has changed significantly in the last 30 years. 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