A Conservation Paradox for the 21St Century: the European Wild Rabbit Oryctolagus Cuniculus, an Invasive Alien and an Endangered Native Species

Mammal Rev. 2008, Volume 38, No. 4, 304–320. Printed in Singapore.

A conservation paradox for the 21st century: the European wild rabbit Oryctolagus cuniculus, an invasive alien and an endangered native species

ALEXANDER C. LEES* and DIANA J. BELL† *Centre for Ecology, Evolution and Conservation, School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK, and †Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK

ABSTRACT 1. This review highlights the status of the European wild rabbit Oryctolagus cuniculus, which is threatened within its native range and yet is a highly successful colonizer across its worldwide, introduced range. 2. The European wild rabbit is a keystone species in Iberia, and the survival of a range of threatened predator species, including the Iberian lynx Lynx pardinus and Spanish imperial eagle Aquila aldabertii, is dependent upon the restoration of rabbit populations. Although not native to the UK, the rabbit also performs signiﬁcant ecosystem services for nationally rare UK species, by maintaining short sward heights in heathland and grassland ecosystems, and serving as a prey item for populations of predators. 3. We identify the European wild rabbit as an excellent model to demonstrate the wide range of complex effects that an introduced mammalian species may exert on ecosystems to which it has been introduced. These effects include habitat degradation following overgrazing, competition with native mammals and facilitating meso-predator release and hyperpredation. 4. We also show that rabbit eradication from some sites may generate more problems than are solved because of the impacts of trophic cascades stemming from dependence on rabbits by native predator assemblages.

Keywords: biological control, habitat management, myxomatosis, non-native, reintroduction

Mammal Review (2008), 38, 304–320 doi: 10.1111/j.1365-2907.2008.00116.x

INTRODUCTION The introduction of alien species, deliberate or accidental, into new ecosystems threatens the integrity and diversity of those communities and represents one of the most potent threats to biodiversity worldwide (e.g. Williamson, 1996; Mooney & Hobbs, 2000; Gaston et al., 2003). The European wild rabbit Oryctolagus cuniculus is one of the most successful invasive mammals. Ancestors from its native Iberian range have been introduced to every continent except Antarctica and over 800 different islands or island groups, although with mixed success (Flux & Fullagar, 1992; Flux, 1994). In stark contrast, a combination of introduced pathogens (including Myxoma virus and rabbit calicivirus), overhunting, habitat loss and changes in land use have caused a serious decline in rabbit populations across the Iberian Peninsula where the species is an important prey item for over 40 vertebrate predators,

Correspondence: D. J. Bell. E-mail: [email protected]

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 Rabbit conservation and eradication problems 305 including the globally endangered Iberian lynx Lynx pardinus and Spanish imperial eagle Aquila aldabertii (Delibes & Hiraldo, 1981; Fa, Sharples & Bell, 1999; Ferrer & Negro, 2004). In an attempt to save these predators from extinction, the European rabbit has become the subject of intensive conservation efforts in Spain and Portugal (e.g. Villafuerte & Moreno, 1997; Virgos et al., 2003; Angulo & Villafuerte, 2004; Moreno et al., 2004; Calvete, Angulo & Estrada, 2005). Elsewhere, within its new range, introduction of the European rabbit has perturbed communities in varying manners by altering the composition and local abundance of both ﬂora and fauna. Trophic-cascade effects initiated by rabbit introduction often threaten the stability of insular ecosystems, but after a new balance has been achieved, rabbit removal may have further detrimental effects on such communities. This paper reviews these impacts and highlights factors that might predispose this species to success as an invasive exotic mammal. We evaluate the measures taken to mitigate or eliminate the European rabbit’s impact within its new range and ﬁnally highlight lessons learned from this species which may have broader application for the management of other invasive taxa.

EUROPEAN RABBIT ECOLOGY AND EFFECTS ON COMMUNITY STRUCTURE WITHIN EUROPE Rabbit taxonomy and ecology in Iberia Here we review the ecology of European rabbits in order to assess the characteristics that both predispose them for success as an introduced species and place them at risk within their native range. Pleistocene fossil records indicate that the rabbit was widely distributed across Europe prior to the final glaciations of the last ice age (Corbet, 1986), after which its range contracted to refugia on the Iberian Peninsula (Gibb, 1990; Flux, 1994; Thompson, 1994). Recent genetic analysis indicates several distinct subspecies: the smaller O. c. algirus is found in southern Spain and on the Atlantic Islands of the Azores, Madeira and Porto Santo, while the larger O. c. cuniculus is distributed across northern Spain and southern France and gave rise to the introduced populations found in the UK, central Europe and Australia (Sharples, Fa & Bell, 1996; Branco, Ferrand & Monnerot, 2000; Branco et al., 2002). Other subspecies are recognized on Atlantic and Mediterranean Islands where O. c. huxlei of Sicily and Sardinia may be endangered (Mitchell-Jones et al., 1999). Rabbit distribution is closely associated with vegetation cover and soil type in Iberia where oak savannah (dehesas) and grassland mattoral are the preferred habitat types. European rabbits tend to avoid cold and wet ecotypes and may not be able to live over 1500 m (Angulo et al., 1998; Fa et al., 1999). Although the rabbit may include a range of species in its diet, grasses and forbs are preferred and there may be local specialization on a few selected species (Rogers, Arthur & Soriguer, 1994). The degree of sociality, which in turn influences group structure and mating systems, varies according to population density and habitat and substrate types. Group living tends to occur where the availability of suitable burrowing habitats is limited and it is in these circumstances that the species lives in territorial, warren-based, breeding groups containing 3–20 individuals (mean 4) (Villafuerte & Moreno, 1997). Predation pressure is hypothesized to have been the ultimate cause for group living, the burrows (warrens) providing a place to retreat from avian and terrestrial mammalian predators (Villafuerte & Moreno, 1997). Other benefits to group living could arise from including cooperative construction and maintenance of the group warren (Ebenspherger & Cofre, 2001), thermoregulation (Bell, 1983; Canals, Rosenmann & Bozinovic, 1997; Allaine, 2000) and desirable changes in the quality of food produced by group foraging effects (Bell, 1983; Thompson, 1994; Van de Koppel et al., 1996). Within breeding groups, both sexes exhibit intrasexual, linear dominance hierarchies, with

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 306 A. C. Lees and D. J. Bell reproductive success biased towards the high-ranking individuals. Each sex helps to defend a group territory, the females competing for access to warrens and the males in turn competing for access to females (Bell, 1983, 1986). Inbreeding avoidance is achieved via a trend towards male dispersal and female philopatry, the latter acting to increase relatedness between females within groups, possibly fostering the evolution of kin-biased reciprocity (Webb et al., 1995). Intense predation pressure has selected for high fecundity in rabbits: females are capable of reproducing in their ﬁrst year and average annual litter sizes in southern Europe are around 10–13, with higher productivity in the north (Rogers et al., 1994; Bell, 1999). Population size is limited by climate (thermal limits, rainfall, and vegetation quality and quantity), terrain (available substrate for burrowing and soil type suitable for their major food species), predation pressure (density and diversity of predators) and more recently, introduced pathogens (Bell & Webb, 1991; Fa et al., 1999; Wilkinson, 2004; Calvete, 2006).

The role of the rabbit as a keystone species in Iberian ecosystems The European wild rabbit plays a major role both directly and indirectly in ecosystem services in south-west Europe and is also of economic importance as a game species (Fa et al., 1999; Angulo & Villafuerte, 2004). Nevertheless, its ecology in this region has only recently come under intensive study. Rabbits are highly selective grazers and at moderate densities they can produce mosaics of differing vegetation, thereby increasing floral and faunal species richness (Ausden & Treweek, 1995). They also make significant localized contributions to soil fertility and may therefore be important in establishing and maintaining plant cover (Willott et al., 2000). In addition, they may also play an important role in seed dispersal, although this has yet to be fully investigated (Rogers et al., 1994). However, it is the rabbit’s role as a keystone prey item in Spain and Portugal that has been at the forefront of most recent research on the species. Over 40 different vertebrate predators include European wild rabbits in their diet (Delibes & Hiraldo, 1981) including two globally endangered species, the Iberian lynx and Spanish imperial eagle which prey almost exclusively on them (Palomares et al., 2001; Ferrer et al., 2003). This specialization on a single prey species with a declining population has brought these two ecologically similar taxa to the brink of extinction in the 21st century (Ferrer & Negro, 2004). Rabbits are also an important prey item for other well-studied species of conservation concern, forming 74% of the total consumed biomass for the Iberian wild cat Felis silvestris tartessia and 35% for Bonelli’s eagles Hieraaetus fasciatus (Gil- Sanchez, Valenzuela & Sanchez, 1999; Ontiveros & Pleguezuelos, 2000). Such dependence on rabbits forces niche segregation between these carnivores; red foxes Vulpes vulpes, for instance, avoid lynx (which will kill foxes) by hunting in habitats not frequented by lynx, while European badgers Meles meles are tolerated by lynx probably because they compete less with them (Fedriani, Palomares & Delibes, 1999). Lynx also regulate populations of Egyptian mongooses Herpestes ichneumon, an example of meso-predator suppression of potential economic benefit to rabbit hunters as total rabbit biomass consumed by predators is reduced (Palomares et al., 1995). The impact of introduced Brazilian Myxoma virus (from its natural host, the Brazilian forest rabbit Sylvilagus brasiliensis) on Iberian rabbit populations is not well documented (Wilkinson, 2004), but the arrival of a relatively new viral disease, rabbit haemorrhagic disease (RHD) (Liu et al., 1984), also referred to as rabbit calicivirus, has contributed to a significant decline in rabbit abundance (Blanco & Villafuerte, 1993; Villafuerte et al., 1994; Fa et al., 1999, 2001; Calvete, 2006). The knock-on effects of the latter have resulted in a trophic cascade, which threatens the existence of some of the rarer top predators (Villafuerte et al., 1995; Fa et al., 1999). Eagle owls Bubo bubo, another rabbit specialist, failed to breed

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 Rabbit conservation and eradication problems 307 after a crash in rabbit prey populations following an RHD outbreak, but managed to persist in the area by diet-switching to western hedgehogs Erinaceus europaeus and red-legged partridges Alectoris rufa (Martinez & Zuberogoitia 2001; Penteriani, Gallardo & Roche, 2002). Levels of eagle owl predation on raptors have also been found to be negatively correlated with that on rabbits, which may be interpreted either as evidence of competitor removal or food stress (Serrano, 2000). A crash in rabbit populations associated with RHD can also generate competition between native predators and humans, resulting in increased persecution of raptors for fear of competition (Villafuerte, Vinuela & Blanco, 1998). Calvete et al. (2005) applied a seasonal modelling approach to rabbit population dynamics in Iberia to assess the sustainability of current hunting regimes and concluded that the maintenance of the current main rabbit-hunting season during the Autumn–Winter period was the most conservative option for the harvesting of wild rabbit populations. Under pressure from habitat loss, viral diseases, overhunting and living under intense natural predation pressure, rabbit populations continue to decrease. Spanish and Portuguese conservationists face an uphill struggle to preserve this rabbit-dependent ecosystem and restocking measures now top the list of management techniques, but with apparently little success (Alves et al., 1998; Moreno et al., 2004; Calvete, 2006).

History of the rabbit in the UK and its effect on native communities Formerly a member of the British mammal fauna during at least one interglacial in the mid-Pleistocene (Stuart, 1974; Thompson, 1994), the rabbit was extirpated as a native during one of the later glacial periods (Gibb, 1990; Flux, 1994; Thompson, 1994). The species was not reintroduced into the UK until after the Norman conquest, with the first releases in the 12th and 13th centuries on islands and coastal sites with favourable substrates for burrowing (Sheail, 1971; Flux, 1994). On the mainland, rabbits remained rare in the wild until the onset of a combination of significant changes in habitat management during the 19th century. These management changes included the intensive control of native mammalian and avian predators to protect game species for hunting, together with landscape changes associated with contemporaneous major agricultural reform (e.g. sowing of winter fodder crops and the planting of hedgerows), which offered rabbits both food and shelter in winter (Sheail, 1971; Thompson, 1994). Under such favourable circumstances, UK rabbit numbers increased to an estimated peak of between 60 and 100 million in the early 1950s (Sheail, 1971) when the species was considered a major agricultural pest (Cowan, 1991). The release of myxomatosis as a biological control agent in 1953 resulted in an initial mortality of at least 99%, although there was no evidence of local extinctions (Hudson, Thompson & Mansi, 1955; Cowan, 1991). Subsequently, there was a partial population recovery associated with selection for attenuation of the disease and genetic resistance in the rabbits, but numbers today are still at less than 40% of pre-crash levels (Fenner & Ross, 1994; Harris et al., 1995). The introduction of rabbits and their intensive grazing regimes profoundly affected the character of much of the British countryside. The effect was perhaps most marked on islands, a pattern which would later be reflected over large parts of the world. Unchecked by predators or man, rabbit populations on Lundy Island in the Bristol Channel left the island ’incorrigibly barren’ in the 17th and 18th centuries (Sheail, 1971). Grazing pressure resulted in the endemic Lundy cabbage Coincya wrightii and consequently the endemic bronze Lundy cabbage flea beetle Psyliodes luridipennis being restricted to inaccessible cliff-side refugia (Compton, Key & Key, 2002). Overgrazing by rabbits led to depauperate floral communities

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 308 A. C. Lees and D. J. Bell on other islands around this time and many would only recover after the impact of myxomatosis (Sumption & Flowerdew, 1985; Flux & Fullagar, 1992). On the mainland, however, the importance of rabbits in maintaining desirable plant communities and floristic diversity is now well recognized (e.g. Manchester & Bullock, 2000). This role is counter-intuitive given that the species is not native to Britain but such grazing regimes were perhaps regulated originally by large native herbivores and later by domestic livestock. Intermediate rabbit grazing pressure on grassland communities produces the highest species diversity by maintaining a low sward height and preventing succession (Ranwell, 1972). In the UK, such rabbit grazing is significant in the management of fen, grass heath and chalk grassland habitats (Thompson, 1994). Barham & Stewart (2005) investigated the impact of different grazing regimes on the leafhopper community on chalk heath in southern England and found that plots grazed only by rabbits had a leafhopper assemblage distinct (species abundance not composition) from either that on ungrazed or mixed-grazing plots. This suggests that the subtle effects of grazing on grassland invertebrate assemblages are not necessarily predictable from an examination of the species composition of the vegetation. The role of rabbits in top-down control of heathland sward height was demonstrated most vividly after the outbreak of myxomatosis. In the absence of intensive rabbit grazing pressure, there was rapid succession by ericaceous shrubs and the development of a new heathland community and associated acidification of soil substrate by gorse Ulex sp. (Grubb & Suter, 1971). Many short-sward specialist invertebrates can only persist in with the presence of rabbits, the best-known example being the large blue butterfly Maculinea arion. The decline of the large blue butterfly paralleled the loss of rabbits following the arrival of myxomatosis and associated changes in grazing pressure. Its caterpillar is reared by the red ant Myrmica sabuleti, which is itself dependent on short sward heights (Thomas, 1980). The re-expansion of populations of silver-spotted skipper butterfly Hesperia comma has also been attributed to a recovery of local rabbit populations (Davies et al., 2005). Birds of conservation concern relying on rabbit-dependent habitats include the stone curlew Burhinus oedicnemus, red-billed chough Pyrrhocorax pyrrhocorax and woodlark Lullula arborea (Bowden, 1990; Green & Griffiths, 1994; McCanch, 2000). Previously, the native herbivore mega-fauna may have maintained the disturbance regimes necessary to create temporary niches for the characteristic species of the East Anglian Brecklands or the Downs of southern England. However, it seems that rabbits are now required to ensure the survival of such specialists at sites, which are constantly heavily grazed within a hyper- fragmented, anthropogenic landscape which only leaves space for a small number of refugia. Indirect beneficial effects on other species of high local rabbit populations include increased reproductive success in the stone curlew, where nest predation by foxes was inversely related to rabbit abundance (Bealey et al., 1999). Elsewhere in the UK, the rabbit has also become a significant prey item for a number of native predators including western polecats Mustela putorius, European wild cats Felis silvestris, red kites Milvus milvus and common buzzards Buteo buteo in a manner analogous to its role in Iberia (Bell, 1995). Many of these species declined following myxomatosis, but this was most marked in the common buzzard (Sim et al., 2001). The indirect effects of myxomatosis were sometimes recorded in predators which do not feed on rabbits; e.g. reproductive success of tawny owls Strix aluco declined in Wytham Woods, Oxford as a result of increased competition with stoats Mustela erminea and red foxes for its small mammal prey base (Southern, 1970). For a fuller review of the ecological effects following myxomatosis, see Sumption & Flowerdew (1985). Human attitudes towards rabbits in the UK have changed markedly over time (Sheail, 1991), and consideration of their removal from the UK would

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 Rabbit conservation and eradication problems 309 not only be prohibitively expensive and logistically unfeasible, but may also have more negative than positive impacts on biodiversity. This development represents an interesting new conservation paradigm; contemporary conservation policy typically advocates the removal of non-native species so that the community might return to its original equilibrium (IUCN, 2000). However, rabbits have become a key component of the British countryside maintaining habitats that were previously maintained by species that have either become totally or at least functionally extinct.

THE ECOLOGY AND IMPACT OF EUROPEAN RABBITS AS AN INVASIVE INTRODUCED SPECIES Beyond their native range in Western Europe, rabbits have proven to be a highly successful introduced species, their impacts on native communities are many and varied, and the solutions to the problems posed for management agencies are not always self-evident.

Rabbit spread and status outside Western Europe Rabbits of wild origin were ﬁrst liberated in Australia at Geelong, Victoria in 1859 and subsequently spread at an average rate of 54 km a year across that country (Myers, 1971; Myers et al., 1994). Its current distribution is thought to cover most of the Australian continent (Flux, 1994). Rabbits were ﬁrst released successfully in South America in Chile in 1936 and subsequent introductions established populations in the extreme south of the country and around Santiago. From here, the European rabbit spread over the Andes into Argentina to occupy a large area of the latter country (Howard & Amaya, 1975). The only extensive population in North America is centred on the San Juan Islands while North Africa holds what may be either relict or introduced populations in both Morocco and Algeria (Flux, 1994). It is on oceanic islands that the species has really consolidated its global distribution; which now includes around 800 different islands or island groups across the globe, north to 59–62° (e.g. Middleton Island, Alaska), south to 54–55° (e.g. Macquarie Island) and around the equator (e.g. Ascension Island) (Flux, 1994). The limiting factors appear to be depth of snow cover at high latitudes and access to either water or green vegetation at low latitudes, where they can tolerate temperatures as high as 50°C (Flux, 1994).

Effects of herbivory The effect of overgrazing has been arguably the most significant impact of Oryctolagus on native communities. This has invariably resulted in depauperate plant communities; the effects of which can often be felt at all trophic levels (Chapuis, Frenot & Lebouvier, 1994; Eldridge & Myers, 2001). Rabbits are often density-independent grazers, even on the depauperate insular environment of Alegranza Island (Canary Islands), where the habit of selecting certain species has had important consequences for the composition and distribution of the vegetation over the years (Martin, Marrero & Nogales, 2003). Similarly, the succulent Dudleya linearis has been driven close to extinction on the San Benito Islands (Mexico) following the introduction of European wild rabbits which also show a preference for the endemic Malva pacifica (Donlan et al., 2000; Donlan, Tershy & Croll, 2002). The polypha- gous, but hierarchical, diet of rabbits allows them to switch forage species, allowing this herbivore to continue to flourish despite a decrease in preferred plant species (Donlan et al., 2002). Perhaps even more insidiously, under intensive grazing pressure from rabbits, native herbs are being out-competed by introduced Mediterranean herbs with which the rabbits co-evolved (Holmgren et al., 2000). This is an example of a ’Red Queen’ effect (Van Valen,

1973) where an increase in evolutionary fitness in one species fosters an increase in fitness in a prey species or competitor. The response of floral communities to rabbit removal is typically rapid and dramatic; e.g. a sixfold increase in plant yield followed rabbit eradication in a dry tussock grassland community in Central Otago, New Zealand (Norbury & Norbury, 1996). Despite such examples, the removal of rabbits per se may not result in a rapid return of the community present pre-invasion. A tendency towards selection of fast-growing exotic species has been documented following rabbit depopulation in both continental (Norbury, Heyward & Parkes, 2002) and island (North, Bullock & Dulloo, 1994; Chapuis, Frenot & Lebouvier, 2004) ecosystems. Following a release from top-down control, these exotic plants may then impact on both agriculture and the survival of the remnant endemic plant communities. At least one endemic plant species present on Round Island, Mauritius appears to have declined following introduced rabbit depopulation, and it has been suggested that rabbit grazing may have maintained this plant following the loss of grazing pressures from, now extinct, native giant tortoises (C. Jones, pers. comm.). In order to assess the impact of rabbit herbivory should the potential of competitor release be suspected, the experimental use of rabbit exclosures would permit an assessment of community composition of the regenerating vegetation. However, although the latter may permit a judgement of the effects on plant succession, there is also a potential for cascade effects influencing other species. Following the removal of rabbits from Macquarie Island, grazing pressure on the native tussock grass Poa foliosa was reduced; this grass is the preferred habitat of the introduced black rat Rattus rattus which brought the rats into contact with burrow-nesting seabirds which had previously escaped rat predation (Abbott, Marchant & Cranfield, 2000).

Direct and indirect competition with native fauna Introduced rabbits impact on native fauna, both directly and indirectly via a range of differing mechanisms which may interact synergistically and result in population crashes or extinctions of native species. Analysis of the historical role of rabbits in the mass extinctions of Australian marsupials suggests that irrespective of their individual life history characteristics, habitat degradation (caused principally by sheep but also aggravated by rabbits) was the main extrinsic factor driving declines (Fisher, Blomberg & Owens, 2003), even if foxes or man added the fatal blow (Dickman et al., 1993). It also seems likely that competition for burrows with rabbits was the decisive factor in the extinction of the Nalpa bilby Macrotis lagotis grandis and the lesser stick-nest rat Leporillus apicalis. Ironically, the massive trapping and poisoning campaigns directed against rabbits in Australia may have represented the final nail in the coffin for many of the marsupials that had been brought to the brink of extinction (Myers et al., 1994). Today, rabbits have been implicated in the declines of Australian mammals as morphologically diverse as macropods including red kangaroos Macropus rufa and rufous hare-wallabys Lagorchestes hirsutus (Lundiejenkins, Corbett & Phillips, 1993; Dawson & Ellis, 1994) and western barred bandicoots Perameles bougainville (Richards & Short, 2003). However, high population densities of European rabbits at the reintroduction site for the burrowing bettong Bettongia lesueur did not appear to be a limiting factor for populations of this species (Short & Turner, 2000) and was probably not a major causal agent for its extinction on the mainland (Robley, Short & Bradley, 2001, 2002). However, some unambiguous examples do exist. Overgrazing by rabbits on Laysan Island (Pacific Ocean) indirectly contributed to the extinction of three bird taxa: the Laysan rail Porzana palmeri, Laysan millerbird Acrocephalus familiaris and Laysan honeycreeper Himateone sanguinea freethii (Fuller, 2001). Similarly, the extinction of an endemic race of the song sparrow Melospiza melodia graminea was attributed to a loss of habitat following the introduction of

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 Rabbit conservation and eradication problems 311 rabbits of domestic origin (Anon, 1983). On the other side of the Paciﬁc in New Zealand, rabbits reduce both the food and cover of the native skinks Oligosoma spp., and also compete indirectly by overgrazing and thus reducing the availability of skink refuges from predators (Norbury, 2001). Examples of community perturbations by rabbits are common on islands, perhaps because these communities are more easily invaded (e.g. Case, 1996; Lonsdale, 1999) or simply easier to study. Some examples can often appear counterintuitive, e.g. rabbit burrows on Enderby Island and Rose Islands (Auckland Group) caused an annual mortality (before rabbit eradication) of up to 10% in New Zealand sea lion Phocartos hookeri pups which were unable to negotiate a rabbit-impacted landscape and became trapped in rabbit burrows (Torr, 2002). Overgrazing at the same site made Auckland Island teal Anas aucklandica and Auckland Island snipe Coenocorypha aucklandica more vulnerable to predation from subantarctic skuas Catharacta antarctica lonnbergi. Rabbits were subsequently eliminated from this site by a poisoning campaign (Torr, 2002). Native species require environmental plasticity in order to adapt to changes in their habitats resulting from the introduction of rabbits. In Australia, rabbits almost caused the extinction of long-billed corellas Cacatua tenuirostris through competition for their preferred food plant, but fortuitously the corellas learned to eat an exotic weed and their distribution is now expanding. However, the same cannot be said for the night parrot Geopsittacus occidentalis which may now be on the verge of extinction following its failure to adapt to rabbit-perturbed landscapes (Bole, Longmore & Thompson, 1994; Snyder et al., 2000). Rabbits differ from other introduced grazing mammals which cause community perturbation through overgrazing in that most of the latter are large ungulates or bovines, e.g. feral goats Capra hircus and feral pigs Sus scrofa. These large-bodied species have a lower fecundity than rabbits and occur at lower densities, thus their complete removal from a region is much more readily achieved than the eradication of rabbits from a comparably sized area. The threat from rabbit herbivory appears to be strongest on small oceanic islands where an introduced population can quickly exhaust the island’s resources before density-dependent effects cause population regulation.

Diet-switching by native predators Theoretically, the introduction of a new prey item into an ecosystem is unlikely to go unnoticed by native carnivores, and this has been demonstrated when rabbits have been introduced onto new continents. Naturalized rabbit populations (which coexist along with introduced European hares Lepus europaeus) in Chile and Argentina were originally largely ignored by native predators (Jaksic´ & Soriguer, 1981). More recent studies have found that rabbits have subsequently become a staple part of native carnivore diets, representing 81.7% biomass of the diet of black-chested eagles Geranoaetus melanoleucus (Pavez, Gonzalez & Jimenez, 1992), 55% for great horned owls Bubo virginianus (Donazar et al., 1997) and 95% for the lesser grison Galictis cuja (Delibes et al., 2003), leading to an increase in abundance of such predators. This specialization in introduced lagomorphs is less surprising when viewed in the context of the massive declines attributed to overhunting of native large-bodied herbivores (e.g. guanacos Lama guanicoe and lesser rheas Pterocnemia pennata) and their ecological extinction as prey species for the native carnivore assemblage. Furthermore, competition for food between the introduced lagomorphs and the native ungulates and ratites may further suppress their recovery (Novaro, Funes & Walker, 2000). With widespread declines and extinction of many marsupial taxa, it is not surprising that native Australian predators, particularly raptors, have switched their diets to rabbits; indeed

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 312 A. C. Lees and D. J. Bell many are now highly dependent on them (Newsome et al., 1997). This specialization can be almost complete as found in wedge-tailed eagles Aquila audax in arid western Australia where rabbits comprised up to 97% of their diet (Ridpath & Brooker, 1986). However, these increases in some predator species have come at the expense of others such as the grey falcon Falco hypoleucos, in this case as a result of rabbit-mediated habitat changes (Mooney, 1998). The European rabbit has not been introduced extensively in North America, perhaps because of the presence of native rabbits of the genus Sylvilagus, but they have been introduced to the San Juan Islands in the USA. Here they have become the second most important food item (after glaucous-winged gulls Larus glaucescens) for bald eagles (Knight et al., 1990) with golden eagles Aquila chrysaetos, red-tailed hawks Buteo jamaicensis and great horned owls also often becoming locally dependent on this prey species (Stevens & Weisbrod, 1979). The rabbit’s impact on native predators on islands have been less well documented, perhaps because island ecosystems tend to be simpler and tend not to support populations of large native predators capable of preying upon rabbits. Nevertheless, there is evidence of a reduction in predation pressure on blue petrels Haloberna caerula by brown skuas Catharacta lonnbergi on the Kerguelen archipelago where the skuas prey extensively on introduced rabbits (Moncorps et al., 1997). Furthermore, on the Canary Islands, carrion of introduced rabbits (and goats) is a mainstay of the diet of island scavengers including endemic races of Egyptian vulture Neophron percnopterus majorensis and common buzzard Buteo buteo insularum following the extinction of their original prey base (Gangoso et al., 2006). The diet-switching paradigm following non-native introductions presents a major challenge to conservation biologists. In most of the above cases, the introduction of rabbits resulted in beneﬁts to the predator community without any documented impact on other prey species. However, this is likely to have resulted from the species being introduced into communities that were already far from equilibrium because of a reduction in the original prey base. Immediate removal of rabbits without any remedial conservation action might result in declines or even local extinction of population of the predator species. If the removal of rabbits is ﬁnancially feasible, then management and reintroduction of the original prey base is critical to ensure the long-term persistence of the dependent predator guild (Zavaleta, Hobbs & Mooney, 2001).

Hyperpredation and meso-predator release The availability of introduced prey can impact negatively on native prey species by the process of hyperpredation, whereby the availability of non-native prey inﬂates populations of introduced (or native) predator populations, which consequently increase predation rates on indigenous species. Much of the research on the hyperpredation problem has emanated from Australia, New Zealand and the Sub-Antarctic islands, all of which lack placental mammalian carnivores. Typical examples include an increased likelihood of nest failure in banded dotterels Charadrius bicinctus in New Zealand in areas of high rabbit population density (Rebergen et al., 1998) and the presence of rabbits as a food source for black rats on Whale Island, New Zealand (Imber, Harrison & Harrison, 2000). In the latter example, this over-winter food resource enables circannual survival of rats permitting them to successfully exploit colonies of grey-faced petrels Pterodroma macroptera gouldi when the latter return to breed. Similarly, the introduction of Másafuera hawks Buteo polysoma exsul onto Robinson Crusoe (Juan Fernández Island group, southern Paciﬁc) to control expanding rabbit populations resulted in hawk predation on two species of Pterodroma petrels and endemic land birds particularly Másafuera rayadito Aphrastura masafuerae (Hahn & Römer, 2002).

Such examples may serve to simplify a more complicated picture, however, since the removal of rabbits or their exotic predators in isolation may exaggerate the problem. Impacts of a three-way interaction between introduced predators, native and non-native prey may also involve the phenomenon of meso-predator release whereby removal of the introduced predator frees introduced prey from top-down control and may facilitate its out-competing of native species. Rabbit numbers are limited by predation from introduced red foxes in Western New South Wales, Australia, while, in turn, dingoes Canis familiaris dingo limit fox numbers (Newsome et al., 2001). Fox removal in SE Australia resulted in a growth of rabbit populations 6.5–12 times their initial population size in 12 months, providing evidence for a serious ecological cost of predator control. Likewise, Courchamp, Langlais & Sugihara (1999a,b) suggested that predator eradication may not always be the optimal management policy to ensure the persistence of population of native species. Feral cats are a scourge of many island groups, preying heavily on endemic birds and mammals and are widely implicated in species extinction (Fuller, 2001). However, the diet of feral cats on many islands has been recorded as being heavily biased towards introduced mammals (e.g. Fitzgerald, 1988; Nogales & Medina, 1996). In such instances, feral cats may regulate rat Rattus spp. numbers and increase success of native species, but where rabbits are present, they will be preyed upon preferentially over rats (Fitzgerald, 1988; Zavaleta et al., 2001), releasing rats from top-down control but suppressing rabbit damage to vegetation. Predation of native skinks Oligosoma spp. by introduced carnivores in New Zealand’s dry grasslands increased markedly after sudden declines in rabbit abundance. Skink predation was found to be inversely density-dependent, thus the rabbit population needs to be maintained at reduced levels or the entire exotic community needs to be extirpated (Norbury, 2001). The patterns and causes of extinction and decline in Australian conilurine rodents suggest a major role for hyperpredation with increased rates of extirpation in areas with elevated densities of introduced mice and rabbits (Smith & Quin, 1996). Furthermore, the extinction of rat-kangaroos (Potoroidae) in New South Wales (and probably other marsupials elsewhere) is ostensibly linked with the arrival of red foxes, whose populations are boosted by the presence of rabbits (Short, 1998; Short, Kinnear & Robey, 2002). Considering these problems, Banks (1999) implemented a field-based predator removal experiment to test the ‘predator limitation/doomed surplus’ hypotheses on the impact of introduced red foxes on populations of native bush rats Rattus fuscipes in SE Australia. There was a general lack of response by rat populations to fox removal, suggestive of the doomed ‘surplus hypothesis’ that predation was compensatory rather than additive. Hence when predation pressure is low, not all mortality is additive and indiscriminate control is unlikely to benefit all prey species involved. Thus control should be directed towards predators when native species are predation-limited or when mortality threatens persistence. The mixed blessing of RHD has also reached Australasia and its affects and potential effects are generating much debate. Modelling RHD outbreaks in semi-arid Australia, Pech & Hood (1998) concluded that whether or not indirect or direct competition with rabbits is involved, a reduction in rabbit numbers leading to a drop in fox populations would ultimately be beneficial for native mammals. In such a case, it will be a matter of ‘weathering the storm’ for the native fauna. Haselmayer & Jamieson (2001) documented increased nesting failure of pukeko Porphyrio porphyrio nests in New Zealand following a crash in rabbit numbers post-RHD, possibly a result of diet switching by a native predator, the Australasian harrier Circus approximans which had become a rabbit specialist. Disentangling these complex interrelationships within novel ecosystems into which a successful invader has been introduced is critical to conserva-

© 2008 The Authors. Journal compilation © 2008 Mammal Society, Mammal Review, 38, 304–320 314 A. C. Lees and D. J. Bell tion planning. Appropriate management guidelines must be assessed on a case-by-case basis and will require quantitative research and predictive modelling.

DISCUSSION The European wild rabbit’s remarkable environmental tolerance of sub-Antarctic to equa- torial temperatures and ability to subsist on as little as ‘seaweed, driftwood and lichens’ (Cranham, 1972) are no doubt attributable to the range of environmental extremes which the species faced during its evolutionary history in Iberia. Thus, it can be suggested that the taxon was ‘pre-adaptated’ to display extreme environmental plasticity within its new range. However, it was not just this tolerance and its generalist nature that helped this species to gain a foothold as a successful invasive. Other factors that may have conspired to promote success have included predator and competitive release, floral changes (e.g. an increase in annuals and decrease in perennials which typically follows extensive anthropogenic disturbance), and possibly reduced parasite loads – a proposition that is worthy of future research. Assessing the best course of action with respect to removal/management of a successful colonizer species like the European rabbit depends on: (i) the species which need to be removed; (ii) the degree to which it has/they have displaced native species; and (iii) the presence of other introduced species, the populations of which may be positively affected by the trophic cascade unleashed following the removal of the original exotic. In order to pre-empt such problems, practitioners must pre-assess each situation to evaluate both trophic interactions (between natives and exotics and among exotics) and the potential functional roles of exotics. This review highlights the European wild rabbit as an excellent model to demonstrate the range of complex effects that an introduced mammalian species may exert on ecosystems into which it has been introduced. We also highlight the difficult decisions conservation biologists face regarding the fate of this species within its new range where these are confounded by predicting the consequences of further cascade reactions following its removal. It is ironic that we are simultaneously neither able to conserve (in its native range) nor eliminate (in its introduced range) a species for which we know almost everything about its biology and natural history (cf. Simberloff, 2003). The European rabbit may be unique in this position – no other vertebrate is both a threatened keystone community member in one location and a destructive exotic in another. It still remains somewhat unclear why the European rabbit population in Iberia is failing to recover despite intense conservation efforts and despite the adaptability that the species displays elsewhere as an exotic. Habitat degradation and overhunting are the most likely causes in this finely balanced system, where these anthropogenic threats may be tipping the species over the edge, a process accentuated by high natural mortality rates following high predation pressure. Failure to restore rabbit populations, and rabbit-dependent ecosystems across its native Iberian peninsular would represent a major failure for the international conservation community while those charged with attempting to eradicate introduced species should be alerted to the variety of cascade effects which may occur for target species of which far less is known about their ecology. Furthermore, as was opportunely highlighted by Angulo & Cooke (2002), it would be wise not to choose to use genetically modified Myxoma viruses in the eradication of the European rabbit. If these strains were to find their way to European shores (and the lessons learnt from the initial spread of the Myxoma virus suggests they would), then the possibility of the extinction of Oryctolagus there and the potential for a subsequent extinction spasm of rabbit-dependent species remains a distinct possibility.

ACKNOWLEDGEMENTS We would like to thank Toby Gardner and James Gilroy for comments on the manuscript.

REFERENCES Abbott, I., Marchant, N., & Cranfield, R. (2000) Long-term change in the floristic composition and vegetation structure of Carnac Island, Western Australia. Journal of Biogeography, 27, 333–346. Allaine, D. (2000) Sociality, mating systems and reproductive skew in marmots: evidence and hypotheses. Behavioural Processes, 51, 21–34. Alves, P.C., Loureiro, A., Queirós, F., Correia, R., Martins, P., Gonçalves, H. & Pires, J.P. (1998) Wild Rabbit, Orytolagus cuniculus, Restocking Operations in Portugal. Abstract. Euro-American Mammal Congress, Universidade de Santiago de Compostela, Santiago de Compostela, Spain. Angulo, E. & Cooke, B. (2002) First synthesize new viruses then regulate their release? The case of the wild rabbit. Molecular Ecology, 11, 2703–2709. Angulo, E. & Villafuerte, R. (2004) Modelling hunting strategies for the conservation of wild rabbit populations. Biological Conservation, 115, 291–301. Angulo, E., Jordán, G., Blanco, J.C. & Villafuerte, R. (1998) Factors Influencing Rabbit Distribution in Spain. Abstract. Euro-American Mammal Congress, Universidade de Santiago de Compostela, Santiago de Compostela, Spain. Anon (1983) Santa Barbara Song Sparrow. Oryx, 17, 98. Ausden, M. & Treweek, J. (1995) Grasslands. In: Managing Habitats for Conservation (Ed. by W.J. Sutherland & D.A. Hill), pp. 199–299. Cambridge University Press, Cambridge, UK. Banks, P.B. (1999) Predation by introduced foxes on native bush rats in Australia: do foxes take the doomed surplus? Journal of Applied Ecology, 36, 1063–1071. Barham, D. & Stewart, A.J.A. (2005) Differential indirect effects of excluding livestock and rabbits from chalk heath on the associated leafhopper (Hemiptera: Auchenorrhyncha) fauna. Journal of Insect Conservation, 9, 351–361. Bealey, C.E., Green, R.E., Robson, R., Taylor, C.R. & Winspear, R. (1999) Factors affecting the numbers and breeding success of stone curlews Burhinus oedicnemus at Porton Down, Wiltshire. Bird Study, 46, 145–156. Bell, D.J. (1983) Mate choice in the European rabbit. In: Mate Choice (Ed. by P. G. Bateson), pp. 211–223. Cambridge University Press, Cambridge, UK. Bell, D.J. (1986) Social effects on physiology in the European wild rabbit. Mammal Review, 16, 131–137. Bell, D.J. (1995) Habitat management news – rabbit viral haemorrhagic disease. British Wildlife, 6, 177– 178. Bell, D.J. (1999) The European wild rabbit. In: The UFAW Handbook on the Care and Management of Laboratory Animals (Ed. by T. Poole), pp. 387–394. Blackwells, Oxford, UK. Bell, D.J. & Webb, N.J. (1991) Effects of climate on reproduction in the European wild rabbit. Journal of Zoology, 224, 639–648. Blanco, J.C. & Villafuerte, R. (1993) Factores ecologicos que influyen sobre las poblaciones de conejos. Incidencia de la enfermedad hemorrágica. Empresa de Tranformacion Agraria, S.A., Madrid, Spain. Bole, W.E., Longmore, N.W. & Thompson, M.C. (1994) A recent specimen of the night parrot. Geopsittacus- occidentalis. Emu, 94, 37–40. Bowden, C.G.R. (1990) Selection of foraging habitat by woodlarks (Lullula arborea) nesting in pine planta- tions. Journal of Applied Ecology, 27, 410–419. Branco, M., Ferrand, N. & Monnerot, M. (2000) Phylogeography of the European rabbit (Oryctolagus cuniculus) in the Iberian Peninsula inferred from RFLP analysis of the cytochrome b gene. Heredity, 85, 307–317. Branco, M., Monnerot, M., Ferrand, N. & Templeton, A.R. (2002) Postglacial dispersal of the European rabbit (Oryctolagus cuniculus) on the Iberian peninsula reconstructed from nested glade and mismatch analyses of mitochondrial DNA genetic variation. Evolution, 56, 792–803. Calvete, C. (2006) Modeling the effect of population dynamics on the impact of rabbit hemorrhagic disease. Conservation Biology, 20, 1232–1241. Calvete, C., Angulo, E. & Estrada, R. (2005) Conservation of European wild rabbit populations when hunting is age and sex selective. Biological Conservation, 121, 623–634. Canals, M., Rosenmann, M. & Bozinovic, F. (1997) Geometrical aspects of the energetic effectiveness of huddling in small mammals. Acta Theriologica, 42, 321–328. Case, T.J. (1996) Global patterns in the establishment and distribution of exotic birds. Biological Conservation, 78, 69–96.

Chapuis, J.L., Bousses, P. & Barnaud, G. (1994) Alien mammals, impact and management in the French Sub-Antarctic islands. Biological Conservation, 67, 97–104. Chapuis, J.L., Frenot, Y. & Lebouvier, M. (2004) Recovery of native plant communities after eradication of rabbits from the sub-antarctic Kerguelen islands, and influence of climate change. Biological Conservation, 117, 167–179. Compton, S.G., Key, R.S. & Key, R.J.D. (2002) Conserving our little Galapagos – Lundy, Lundy cabbage and its beetles. British Wildlife, 13, 184–190. Corbet, G.B. (1986) Relationships and origins of European lagomorphs. Mammal Review, 16, 105–110. Courchamp, F., Langlais, M. & Sugihara, G. (1999a) Cats protecting birds: modelling the meso-predator release effect. Journal of Animal Ecology, 68, 282–292. Courchamp, F., Langlais, M. & Sugihara, G. (1999b) Control of rabbits to protect island birds from cat predation. Biological Conservation, 89, 219–225. Cowan, D.P. (1991) The European wild rabbit Oryctolagus cuniculus.In:The Handbook of British Mammals (Ed. by G.B. Corbet & S. Harris), pp. 146–154. Blackwell Scientific Publications, Oxford, UK. Cranham, J. (1972) Farne Island rabbits. Animals, 14: 244–245. Davies, Z.G., Wilson, R.J., Brereton, T.M. & Thomas, C.D. (2005) The re-expansion and improving status of the silver-spotted skipper butterfly (Hesperia comma) in Britain: a metapopulation success story. Biological Conservation, 124, 189–198. Dawson, T.J. & Ellis, B.A. (1994) Diets of mammalian herbivores in Australian shrublands – seasonal effects on overlap between red kangaroos, sheep and rabbits on dietary niche breadths and selectivities. Journal of Arid Environments, 26, 257–271. Delibes, M. & Hiraldo, F. (1981) The rabbit as prey in the Iberian Mediterranean ecosystem. In: Proceedings of the World Lagomorph Conference, Guelph, 1979 (Ed. by C.D. MacInnes & K. Myers), pp. 614–622. University of Guelph, Guelph, Canada. Delibes, M., Travaini, A., Zapata, S.C. & Palomares, F. (2003) Alien mammals and the trophic position of the lesser grison Galictis cuja in Argentinian Patagonia. Canadian Journal of Zoology, 81, 157–162. Dickman, C.R., Pressey, R.L., Lim, L. & Parnaby, H.E. (1993) Mammals of particular conservation concern in the western division of New South Wales. Biological Conservation, 65, 219–248. Donazar, J.A., Travaini, A., Ceballos, O., Delibes, M. & Hiraldo, F. (1997) Food habits of the great horned owl in northwestern Argentine Patagonia: the role of introduced lagomorphs. Journal of Raptor Research, 31, 364–369. Donlan, C.J., Tershy, B.R., Keitt, B.S., Wood, B., Sanchez, J.A., Weinstein, A., Croll, D.A. & Alguilar, J.L. (2000) Island conservation action in northwest Mexico. In: Proceedings of the Fifth California Islands Symposium (Ed. by D.H. Browne, H. Chaney & K. Mitchell), pp. 330–338. Santa Barbara Museum of Natural History, Santa Barbara, CA, USA. Donlan, C.J., Tershy, B.R. & Croll, D.A. (2002) Islands and introduced herbivores: conservation action as ecosystem experimentation. Journal of Applied Ecology, 39, 235–246. Ebenspherger, L.A. & Cofre, H. (2001) On the evolution of group-living in the New World cursorial hystricognath rodents. Behavioral Ecology, 12, 227–236. Eldridge, D.J. & Myers, C.A. (2001) The impact of warrens of the European rabbit (Oryctolagus cuniculus L.) on soil and ecological processes in a semi-arid Australian woodland. Journal of Arid Environments, 47, 325–337. Fa, J.E., Sharples, C.M. & Bell, D.J. (1999) Habitat correlates of European rabbit distribution in southern Spain. Journal of Zoology, 249, 83–96. Fa, J.E., Sharples, C.M., Bell, D.J. & Angelis, D. (2001) An individual-based model of rabbit viral haemorrhagic disease in the European wild rabbit. Ecological Modelling, 144, 121–138. Fedriani, J.M., Palomares, F. & Delibes, M. (1999) Niche relations among three sympatric Mediterranean carnivores. Oecologia, 121, 138–148. Fenner, R. & Ross, J. (1994) Myxomatosis. In: The European Rabbit: The History and Biology of a Successful Colonizer (Ed. by H.V. Thompson & C.M. King), pp. 205–239. Oxford University Press, Oxford, UK. Ferrer, M. & Negro, J.J. (2004) The near extinction of two large European predators: super-specialists pay a price. Conservation Biology, 18, 344–349. Ferrer, M., Penteriani, V., Balbontin, J. & Pandolfi, M. (2003) The proportion of immature breeders as a reliable early warning signal of population decline: evidence from the Spanish imperial eagle in Donana. Biological Conservation, 114, 463–466. Fisher, D.O., Blomberg, S.P. & Owens, I.P.F. (2003) Extrinsic versus intrinsic factors in the decline and extinction of Australian marsupials. Proceedings of the Royal Society of London B, 270, 1801–1808. Fitzgerald, B.M. (1988) Diet of domestic cats and their impact on prey populations. In: The Domestic Cat: The Biology of its Behaviour (Ed. by D.C. Turner), pp. 123–146. Cambridge University Press, Cambridge, UK.

Flux, J.E.C. (1994) World distribution. In: The European Rabbit: The History and Biology of a Successful Colonizer (Ed. by H.V. Thompson & C.M. King), pp. 8–21. Oxford University Press, Oxford, UK. Flux, J.E.C. & Fullagar, P.J. (1992) World distribution of the rabbit, Oryctolagus cuniculus, on islands. Mammal Review, 22, 151–205. Fuller, E. (2001) Extinct Birds. Revised Edition. Comstock Publishing Associates, Ithaca, NY, USA. Gangoso, L., Donázar, J.A., Scholz, S., Palacios, C.J. & Hiraldo, F. (2006) Contradiction in conservation of island ecosystems: plants, introduced herbivores and avian scavengers in the Canary Islands. Biodiversity and Conservation, 15, 2231–2248. Gaston, K.J., Jones, A.G., Hänel, C. & Chown, S.L. (2003) Rates of species introduction to a remote oceanic island. Proceedings of the Royal Society of London Series B Biological Sciences, 270, 1091–1098. Gibb, J.A. (1990) The European rabbit Oryctolagus cuniculus. In: Rabbits, Hares and Pikas Status Survey and Conservation Action Plan (Ed. by J.A. Chapman & J.E.C. Flux), pp. 116–120. IUCN, Gland, Switzerland. Gil-Sanchez, J.M., Valenzuela, G. & Sanchez, J.F. (1999) Iberian wild cat Felis silvestris tartessia predation on rabbit Oryctolagus cuniculus: functional response and age selection. Acta Theriologica, 44, 421–428. Green, R.E. & Griffiths, G.H. (1994) Use of preferred nesting habitat by stone curlews Burhinus oedicnemus in relation to vegetation structure. Journal of Zoology, 233, 457–471. Grubb, P.J. & Suter, M.B. (1971) The mechanism of acidification of soil by Calluna and Ulex and the significance for conservation. In: The Scientific Management of Animal and Plant Communities for Conser- vation (Ed. by E. Duffey & A.S. Watt), pp. 115–133. Blackwell Scientific Publications, Oxford, UK. Hahn, I. & Römer, U. (2002) Threatened avifauna of the Juan Fernández archipelago, Chile: the impact of introduced mammals and conservation priorities. Cotinga, 17, 66–72. Harris, S., Morris, P., Wray, S. & Yalden, D. (1995) A Review of British Mammals: Population Estimates and Conservation Status of British Mammals Other than Cetaceans. Joint Nature Conservation Committee, Peterborough, UK. Haselmayer, J. & Jamieson, I.G. (2001) Increased predation on pukeko eggs after the application of rabbit control measures. New Zealand Journal of Ecology, 25, 89–93. Holmgren, M., Avilés, A., Sierralta, L., Segura, A.M. & Fuentes, E.R. (2000) Why have European herbs so successfully invaded the Chilean matorral? Effects of herbivory, soil nutrients, and fire. Journal of Arid Environments, 44, 197–211. Howard, W.E. & Amaya, J.M. (1975) European rabbit invades western Argentina. Journal of Wildlife Management, 39, 757–761. Hudson, J.R., Thompson, H.V. & Mansi, W. (1955) Myxoma virus in Britain. Nature, 176, 783. Imber, M., Harrison, M. & Harrison, J. (2000) Interactions between petrels, rats and rabbits on Whale Island, and effects of rat and rabbit eradication. New Zealand Journal of Ecology, 24, 153–160. IUCN (2000) Guidelines for the Prevention of Biodiversity Loss due to Biological Invasion. IUCN – the World Conservation Union, Gland, Switzerland. Jaksic´, F.M. & Soriguer, R.C. (1981) Predation upon the European rabbit (Oryctolagus cunciculus)inthe mediterranean habitats of Chile and Spain: a comparative analysis. Journal of Animal Ecology, 50, 269–281. Knight, R.L., Randolph, P.J., Allen, G.T., Young, L.S. & Wigen, R.J. (1990) Diets of nesting bald eagles, Haliaeetus leucocephallus, in western Washington. Canadian Field-Naturalist, 104, 545–551. Liu, S.J., Xue, H.P., Pu, B.Q. & Quian, N.H. (1984) A new viral disease in rabbits [In Chinese]. Animal Husbandry and Veterinary Medicine, 16, 253–255. Lonsdale, W.M. (1999) Global patterns of plant invasions and the concept of invisibility. Ecology, 80, 1522–1536. Lundiejenkins, G., Corbett, L.K. & Phillips, C.M. (1993) Ecology of the rufous hare-wallaby, Lagorchestes hirsutus Gould (Marsupialia, Macropodidae), in the Tanami Desert, Northern Territory. 3. Interactions with introduced mammal species. Wildlife Research, 20, 495–511. McCanch, N. (2000) The relationship between red-billed chough Pyrrhocorax pyrrhocorax (L) breeding populations and grazing pressure on the Calf of Man. Bird Study, 47, 295–303. Manchester, S.J. & Bullock, J.M. (2000) The impacts of non-native species on UK biodiversity and the effectiveness of control. Journal of Applied Ecology, 37, 845–864. Martin, M.C., Marrero, P. & Nogales, M. (2003) Seasonal variation in the diet of wild rabbits Oryctolagus cuniculus on a semi-arid Atlantic island (Alegranza, Canarian Archipelago). Acta Theriologica, 48, 399– 410. Martinez, J.A. & Zuberogoitia, I. (2001) The response of the eagle owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease. Journal of fur Ornithologie, 142, 204–211. Mitchell-Jones, A.J., Amori, G., Bogdanowicz, W., Krystufek, B., Reijnders, P.J.H., Spitzenberger, F., Stubbe, M., Thissen, J.B.M., Vorhralik, V. & Zima, J. (1999) The Atlas of European Mammals. Academic Press, London, UK.

Moncorps, S., Chapuis, J.L., Haubreux, D. & Bretagnolle, V. (1997) Diet of the brown skua Catharacta skua lönnbergi on the Kerguelen archipelago: comparisons between techniques. Polar Biology, 19, 9–16. Mooney, N. (1998) Status and conservation of raptors in Australia’s tropics. Journal of Raptor Research, 32, 4–73. Mooney, H.A. & Hobbs, R.J., eds. (2000) Invasive Species in a Changing World. Island Press, Washington, DC, USA. Moreno, S., Villafuerte, R., Cabezas, S. & Lombardi, L. (2004) Wild rabbit restocking for predator conservation in Spain. Biological Conservation, 118, 183–193. Myers, K. (1971) The rabbit in Australia. In: Proceedings of the Advanced Study Institute on Dynamics (Ed. by P.J. Den Boer & G.R. Gradwell), pp. 478–506. Oosterbeek, Wageningen, The Netherlands. Myers, K., Parer, I., Wood, D. & Cooke, B.D. (1994) The rabbit in Australia. In: The European Rabbit: The History and Biology of a Successful Colonizer (Ed. by H.V. Thompson & C.M. King), pp. 108–157. Oxford University Press, Oxford, UK. Newsome, A.E., Pech, R.P., Smyth, R., Banks, P. & Dickman, C. (1997) Potential Impacts on the Australian Native Fauna of Rabbit Calicivirus Disease. Environment Australia, Canberra, Australia. Newsome, A.E., Catling, P.C., Cooke, B.D. & Smyth, R. (2001) Two ecological universes separated by the Dingo Barrier fence in semi-arid Australia: interactions between landscapes, herbivory and carnivory, with and without dingoes. Rangeland Journal, 23, 71–98. Nogales, M. & Medina, F.M. (1996) A review of the diet of feral domestic cats (Felis catus) on the Canary Islands, with new data from the laurel forest of La Gomera. International Journal of Mammalian Biology, 61, 1–6. Norbury, G. (2001) Conserving dryland lizards by reducing predator-mediated apparent competition and direct competition with introduced rabbits. Journal of Applied Ecology, 38, 1350–1361. Norbury, D.C. & Norbury, G.L. (1996) Short-term effects of rabbit grazing on a degraded short-tussock grassland in central Otago. New Zealand Journal of Ecology, 20, 285–288. Norbury, G., Heyward, R. & Parkes, J. (2002) Short-term ecological effects of rabbit haemorrhagic disease in the short-tussock grasslands of the South Island, New Zealand. Wildlife Research, 29, 599–604. North, S.G., Bullock, D.J. & Dulloo, M.E. (1994) Changes in the vegetation and reptile populations on Round Island, Mauritius, following eradications of rabbits. Biological Conservation, 67, 21–28. Novaro, A.J., Funes, M.C. & Walker, R.S. (2000) Ecological extinction of native prey of a carnivore assemblage in Argentine Patagonia. Biological Conservation, 92, 25–33. Ontiveros, D. & Pleguezuelos, J.M. (2000) Inﬂuence of prey densities in the distribution and breeding success of Bonelli’s eagle (Hieraaetus fasciatus): management implications. Biological Conservation, 93, 19– 25. Palomares, F., Gaona, P., Ferreras, P. & Delibes, M. (1995) Positive effects on game species of top predators – an example with lynx, mongooses and rabbits. Conservation Biology, 9, 295–305. Palomares, F., Delibes, M., Revilla, E., Calzada, J. & Fedriani, J.M. (2001) Spatial ecology of Iberian lynx and abundance of European rabbits in southwestern Spain. Wildlife Monographs, 148, 1–36. Pavez, E.F., Gonzalez, C.A. & Jimenez, J.E. (1992) Diet shifts of black-chested eagles (Geranoaetus melanoleucus) from native prey in European rabbits in Chile. Journal of Raptor Research, 26, 27–32. Pech, R.P. & Hood, G.R. (1998) Foxes, rabbits, alternative prey and rabbit calicivirus disease: consequences of a new biological control agent for an outbreaking species in Australia. Journal of Applied Ecology, 35, 434–453. Penteriani, V., Gallardo, M. & Roche, P. (2002) Landscape structure and food supply affect eagle owl (Bubo bubo) density and breeding performance: a case of intra-population heterogeneity. Journal of Zoology, 257, 365–372. Ranwell, D.S. (1972) Newborough Warren, Anglesey. III. Changes in the vegetation on parts of the dune system after the loss of rabbits by myxomatosis. Journal of Ecology, 48, 385–395. Rebergen, A., Keedwell, R., Moller, H. & Maloney, R. (1998) Breeding success and predation at nests of banded dotterel (Charadrius bicinctus) on braided riverbeds in the central South Island, New Zealand. New Zealand Journal of Ecology, 22, 33–41. Richards, J.D. & Short, J. (2003) Reintroduction and establishment of the western barred bandicoot Perameles bougainville (Marsupialia: Peramelidae) at Shark Bay, Western Australia. Biological Conservation, 109, 181–195. Ridpath, M.G. & Brooker, M.G. (1986) The breeding of the wedge-tailed eagles (Aquila audax) in relation to its food supply in arid western Australia. Ibis, 128, 177–194. Robley, A.J., Short, J. & Bradley, S. (2001) Dietary overlap between the burrowing bettong (Bettongia lesueur) and the European rabbit (Oryctolagus cuniculus) in semi-arid coastal Western Australia. Wildlife Research, 28, 341–349.

Robley, A.J., Short, J. & Bradley, S. (2002) Do European rabbits (Oryctolagus cuniculus) inﬂuence the population ecology of the burrowing bettong (Bettongia lesueur)? Wildlife Research, 29, 423–429. Rogers, P.M., Arthur, C.P. & Soriguer, R.C. (1994) The rabbit in continental Europe. In: The European Rabbit: The History and Biology of a Successful Colonizer (Ed. by H.V. Thompson & C.M. King), pp. 23–63. Oxford University Press, Oxford, UK. Serrano, D. (2000) Relationship between raptors and rabbits in the diet of eagle owls in southwestern Europe: competition removal or food stress? Journal of Raptor Research, 34, 305–310. Sharples, C., Fa, J.E. & Bell, D.J. (1996) Geographical variation in size in the European wild rabbit in western Europe and north Africa. Zoological Journal of the Linnean Society of, 117, 141–158. Sheail, J. (1971) Rabbits and Their History. David & Charles Ltd, Newton Abbot, UK. Sheail, J. (1991) The management of an animal population: changing attitudes towards the wild rabbit in Britain. Journal of Environmental Management, 33, 189–203. Short, J. (1998) The extinction of rat-kangaroos (Marsupialia: Potoroidae) in New South Wales, Australia. Biological Conservation, 86, 365–377. Short, J. & Turner, B. (2000) Reintroduction of the burrowing bettong Bettongia lesueur (Marsupialia: Potoroidae) to mainland Australia. Biological Conservation, 96, 185–196. Short, J., Kinnear, J.E. & Robley, A. (2002) Surplus killing by introduced predators in Australia – evidence for ineffective anti-predator adaptations in native prey species? Biological Conservation, 103, 283–301. Sim, I.M.W., Cross, A.V., Lamacraft, D.L. & Pain, D.J. (2001) Correlates of common buzzard Buteo buteo density and breeding success in the West Midlands. Bird Study, 48, 317–329. Simberloff, D. (2003) How much population biology is needed to manage introduced species? Conservation Biology, 17, 83–92. Smith, A.P. & Quin, D.G. (1996) Patterns and causes of extinction and decline in Australian conilurine rodents. Biological Conservation, 77, 243–267. Snyder, N., McGowan, P., Gilardi, J. & Grajal, A., eds. (2000) Parrots. Status Survey and Conservation Action Plan 2000–2004. IUCN, Gland, Switzerland. Southern, H.N. (1970) The natural control of a population of tawny owls Strix aluco. Journal of Zoology, 162, 197–285. Stevens, W.F. & Weisbrod, A.R. (1979) The biology of the European rabbit on the San Juan Islands, Washington, USA. In: Proceedings of the World Lagomorph Conference, Guelph 1979 (Ed. by K. Myers & C.D. MacInnes), pp. 870–879. University of Guelph, Guelph, Canada. Stuart, A.J. (1974) Pleistocene history of the British vertebrate fauna. Biological Reviews, 49, 225–266. Sumption, K.J. & Flowerdew, J.R. (1985) The ecological effects of the decline of rabbits (Oryctolagus cuniculus) due to myxomatosis. Mammal Review, 15, 151186. Thomas, J.A. (1980) Why did the large blue become extinct in Britain? Oryx, 15, 243–247. Thompson, H.V. (1994) The rabbit in Britain. In: The European Rabbit: The History and Biology of a Successful Colonizer (Ed. by H.V. Thompson & C.M. King), pp. 64–107. Oxford University Press, Oxford, UK. Torr, N. (2002) Eradication or rabbits and mice from subantarctic Enderby and Rose Islands. In: Turning the Tide: The Eradication of Invasive Species (Ed. by C. R. Veitch & M.N. Clout), pp. 319–328. IUCN SSC Invasive Species Specialist Group. IUCN, Cambridge, UK. Van de Koppel, J., Huisman, J., vanderWal, R. & Olff, H. (1996) Patterns of herbivory along a productivity gradient: an empirical and theoretical investigation. Ecology, 77, 736–745. Van Valen, L. (1973) A new evolutionary law. Evolutionary Theory, 1, 1–30. Villafuerte, R. & Moreno, S. (1997) Predation risk, cover type, and group size in European rabbits in Donana (SW Spain). Acta Theriologica, 42, 225–230. Villafuerte, R., Calvete, C., Gortazar, C. & Moreno, S. (1994) First epizootic of rabbit haemorrhagic disease in free-living populations of Orcytolagus cuniculus at Doñana National Park, Spain. Journal of Wildlife Diseases, 30, 176–179. Villafuerte, R., Calvete, C., Blanco, J.C. & Lucientes, J. (1995) Incidence of viral hemorrhagic disease in wild rabbit populations in Spain. Mammalia, 59, 651–659. Villafuerte, R., Vinuela, J. & Blanco, J.C. (1998) Extensive predator persecution caused by population crash in a game species: the case of red kites and rabbits in Spain. Biological Conservation, 84, 181– 188. Virgos, E., Cabezas-Diaz, S., Malo, A., Lozano, J. & Lopez-Huertas, D. (2003) Factors shaping European rabbit abundance in continuous and fragmented populations of central Spain. Acta Theriologica, 48, 113–122. Webb, N.J., Ibrahim, K.M., Bell, D.J. & Hewitt, G.M. (1995) Natal dispersal and genetic-structure in a population of the European wild rabbit (Oryctolagus cuniculus). Molecular Ecology, 4, 239–247.

Wilkinson, D.C. (2004) Population biology, ectoparasites and myxomatosis: a longitudinal study of a free-living population of European wild rabbits (Oryctolagus cuniculus) in East Anglia. Unpublished PhD Thesis, University of East Anglia, Norwich, UK. Williamson, M. (1996) Biological Invasions. Chapman & Hall, London, UK. Willott, S.J., Miller, A.J., Incoll, L.D. & Compton, S.G. (2000) The contribution of rabbits (Oryctolagus cuniculus L.) to soil fertility in semi-arid Spain. Biology and Fertility of Soils, 31, 379–384. Zavaleta, E.S., Hobbs, R.J. & Mooney, H.A. (2001) Viewing invasive species removal in a whole-ecosystem context. Trends in Ecology and Evolution, 18, 454–459.

Submitted 31 July 2006; returned for revision 16 January 2007; revision accepted 11 November 2007 Editor: RM