A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna

Biodivers Conserv (2009) 18:829 846 DOI 10.1007/s10531-008-9503-4 REVIEW PAPER A review on the impacts of feral cats (Felis silvestris catus) in the Canary Islands: implications for the conservation of its endangered fauna Félix Manuel Medina Æ Manuel Nogales Received: 4 February 2008 / Accepted: 8 October 2008 / Published online: 21 October 2008 Ó Springer Science+Business Media B.V. 2008 Abstract Feral cats have been directly responsible for the extinction of numerous species on islands worldwide, including endemic species of mammals, birds and reptiles. The diet of feral cats in the main habitats of the Canary Islands, as generally occurred on oceanic islands, is mainly composed of introduced mammals, and native species of birds, reptiles and insects. The impact of feral cat upon the endangered species was assessed by evaluating their relative abundance in the cats diet and by considering their current conservation status. A total of 68 different preys were identified at species level in all studies carried out in the Canary Islands (5 mammals, 16 birds, 15 reptiles and 32 invertebrates). From all the species preyed by feral cats in the Canary Islands, only four of them are considered threatened by the IUCN Red List of Threatened Species: one endemic bird Saxicola dacotiae and three endemic giant lizards, Gallotia simonyi, Gallotia intermedia, and Gallotia gomerana. Although some efforts on management control have been carried out, it is necessary to enforce these conservation activities on those areas of Tenerife, La Gomera and El Hierro where giant lizards are still present. Furthermore some local areas where endangered bird species are highly predated should be protected. Nevertheless, it is important to take into account the presence of other introduced species such as rats, mice or rabbits in order to avoid problems derived from the hyperpredation process and mesopredator release effect. Keywords Canary Islands Endangered species Felis silvestris catus Food habits Island conservation F. M. Medina (&) Consejería de Medio Ambiente, Cabildo Insular de La Palma, Avenida Los Indianos 20, 28, 38700 Santa Cruz de La Palma, Canary Islands, Spain e-mail: felix.medina@cablapalma.es F. M. Medina M. Nogales Island Ecology and Evolution Research Group (IPNA-CSIC), Astrofísico Francisco Sánchez 3, 38206 La Laguna, Tenerife, Canary Islands, Spain

830 Biodivers Conserv (2009) 18:829 846 Introduction Since its domestication from the African wildcat (Felis silvestris lybica) some 9,000 years ago (Randi and Ragni 1991; Serpell 2000; Driscoll et al. 2007), cats (Felis silvestris catus) has long been associated with humans (Vigne et al. 2004) and has traveled with them to most parts of the world (Fitzgerald 1988). Their generalist behaviour converts this introduced predator into a very adaptable species which is capable of surviving in inhospitable conditions on the most remote oceanic islands (Courchamp et al. 2003). On these, feral cats prey on a high variety of prey, mainly introduced mammals, although they include in their diet an elevate proportion of native birds, reptiles and invertebrate species (Fitzgerald 1988; Fitzgerald and Turner 2000). Oceanic islands are really relevant in the context of whole world biodiversity because harbor an important number of endemic species (Mac Arthur and Wilson 1967; Gorman 1979; Whittaker and Fernández-Palacios 2007). On its, feral cats have been directly responsible for the extinction of numerous mammals (Mellink 1992; Tershy et al. 2002), reptiles (Iverson 1978; Mitchell et al. 2002) and birds (Jehl and Parks 1983; Lever 1994; Veitch 2001). For this reason this predator is considered to be one of the 100 worst invasive species in the world (Lowe et al. 2000). The Canary Islands is an important hotspot of global biodiversity because 2,985 animal and 524 plant species are endemic elements (Martín et al. 2005a). Nevertheless, in the Canaries, at least 1,434 species have been introduced by man and approximately 150 of them are considered such as invasive (Martín et al. 2005a). Cats were probably introduced in the Canary Islands in the fifteenth Century after the European conquest and present feral populations in all the main islands and habitats of the Canarian Archipelago (Nogales et al. 2006; Medina and Nogales 2007). Feral cats are the predator at the top of the food chain, among the vertebrates in these islands (Nogales et al. 1992). The feeding ecology of feral cats on the Canary Islands follows the general pattern of other islands located at similar latitude, being characterized by an important biomass supported by introduced mammals (mainly rabbits and mice) when they are present (Nogales and Medina 1996). However, some specific preys, such as lizards, rats or birds, play an important role in particular habitats in which these prey are available and rather abundant. Historically, feral cats have been considered co-responsible of the extinction of several vertebrate species in the Canaries such as Puffinus holeae, Puffinus olsoni, Pterodroma sp., Carduelis triasi or Emberiza alcoveri although other introduced species such as rats and, overall, the effects of humans by direct consumption and habitat destruction were the most probable cause of their extinction (Rando 2003). These and other extinct species in the Canary Islands such as Gallotia goliath, Canariomys tamarani, C. bravoi or Puffinus olsoni were commonly included in the aborigines diet (Rando 2003). Although the Canary Islands constitute the place where the feral cats diet has been more extensively studied around the world (Nogales et al. 2006), their effect on endemic and endangered species had not been evaluated. For this reason the main aim of this contribution is to review the impact of feral cat upon endemic fauna of these islands, evaluating the conservation status of the different prey items consumed by feral cats in all environments present in this archipelago.

Biodivers Conserv (2009) 18:829 846 831 Materials and methods Study area The Canary Islands are of volcanic origin and are located about 100 km from the northwest coast of Africa. It is composed of seven main islands and several islets (Fig. 1), the highest of which is Tenerife (Pico Teide: 3,718 m a.s.l.) and the lowest Lanzarote (Peñas del Chache: 671 m a.s.l.). Tenerife is the most extensive island (2,034.4 km 2 ), while the smallest is El Hierro (268.7 km 2 ). The climate in the Canaries varies according to altitude and orientation. Mean temperature and annual precipitation ranges from &21 C and 100 300 mm, respectively, in coastal zones, to about 9 C and 500 800 mm, respectively, at higher altitudes. The eastern islands Lanzarote and Fuerteventura, nearest to the African continent, are low in altitude and influenced greatly by dry winds from the nearby Sahara Desert. The vegetation is characterized by a dry xerophytic shrub that only appears in the lowlands of the higher central and western islands of the Canaries (Gran Canaria, Tenerife, La Gomera, El Hierro and La Palma) and is characterized by species of the genus Euphorbia (Euphorbiaceae). The vegetation of the Canaries is clearly distributed as a function of altitude and orientation, including other more humid forest habitats. The vegetation also includes a termophyle forest, located at 300 550 m a.s.l., composed of a mixed wood of Dracaena draco (Agavaceae), Phoenix canariensis (Arecaceae), Juniperus turbinata (Cupressaceae), etc. Between 550 and 1,300 m a.s.l. appears the most humid habitat, the laurel forest, which is constituted by about 20 tree species, several of them endemic. Some of the most relevant species are Laurus novocanariensis and Persea indica (Lauraceae), Myrica faya (Myricaceae) and Erica arborea (Ericaceae), which form a dense evergreen forest. Following in altitude is a dryer monospecific pine forest (1,300 2,000 m a.s.l.) of the endemic Pinus canariensis (Pinaceae), a generally sparse plant formation that shows a scarce understory cover. Finally, above 2,000 m a.s.l., the vegetation is characterized by sparse leguminous shrubs, such as Spartocytisus supranubius and Adenocarpus viscosus (Fabaceae). This last habitat harbors a great component of endemic plants. ATLANTIC OCEAN Montaña Clara Alegranza La Graciosa 29 Lobos LANZAROTE LA PALMA LA GOMERA TENERIFE FUERTEVENTURA 28 EL HIERRO GRAN CANARIA 0 N 15 30 km 18 17 16 15 14 Fig. 1 Map of the Canary Islands showing the localities where the diet of feral cats (Felis silvestris catus) has been studied

832 Biodivers Conserv (2009) 18:829 846 Procedures Although dietary studies could be a poor indicator of impacts on populations (Towns et al. 2006), the study of feral cats diet could be considered as the first step to interpret their impact on prey populations (Paltridge et al. 1997), as had been made in several cases (Seabrook 1990; Chapuis et al. 1994; Donlan et al. 2000; Winter and Wallace 2006). For this reason, the impacts of feral cat in the Canary Islands was reviewed compiling all the studies of feral cats diet in the archipelago and the information found in published and gray literature, including scientific articles, books, and internal reports. Impact of the different prey items captured by feral cats was assessed by evaluating their relative abundance and by considering their respective status at international (IUCN 2007), national (Gobierno de Canarias 2003) and regional levels (Martín et al. 2005b). Results and discussion Cat prey and threatened species A total of 68 different prey were identified at species level in all studies carried out in the Canary Islands (Table 1). From these, five were mammals, 16 birds, 15 reptiles and 32 invertebrates. All mammal prey are introduced species while two bird species are endemic (Phylloscopus canariensis and Fringilla teydea polatzeki), and other five are endemic at subspecies level (Anthus berthelotii berthelotii, Erithacus rubecula superbus, Fringilla coelebs palmae, Parus caeruleus teneriffae, and Sylvia melanocephala leucogastra). Only one of them, Alectoris rufa, is considered such as an introduced species. With regards to reptiles, all of them are endemic from the Canarian Archipelago, these being lizards (the endemic genus Gallotia spp.), geckos (Tarentola spp.) and skinks (Chalcides spp.). From the total of 32 invertebrate species identified in the analysis of feral cat scats in the archipelago, 15 (47%) are endemic. From a conservation point of view, it is also important to consider some results of several studies carried out in the Canaries do not focus on feral cat diet but do on other biological aspects of native birds, such as Bulweria bulwerii, Puffinus assimilis, Hydrobates pelagicus, Saxicola dacotiae and Calandrella rufescens rufescens, which demonstrate important effects of feral cats in their populations (Ardura and Calabuig 1993; Lorenzo et al. 2002; Illera and Díaz 2006). These studies are important when a real knowledge of the effect of feral cats upon native species want to be understood, because bird remains in their faeces did not permit the identification of birds at species level in most of the diet studies carried out in the Canaries (see Nogales and Medina 1996). It is most significant in the case of seabirds because oceanic islands have the most important breeding colonies of seabirds, where the smaller species are especially vulnerable to cat predation (Fitzgerald and Turner 2000; Courchamp et al. 2003). In the Canary Islands the populations of small Procellariiformes species are restricted to uninhabited islets and inaccessible cliffs due to the feral cats pressure (Martín et al. 1989) and currently probably present a lower population sizes than in the past (Rando 2003). From all the species predated by feral cats in the Canary Islands, only four of them are considered such as threatened by the IUCN Red List of Threatened Species (IUCN 2007). The Canary Island Stonechat (Saxicola dacotiae) considered as endangered, and the three giant lizards from the Canaries are included as critically endangered because of the high threat posed by the feral cat predation: Gallotia simonyi from El Hierro

Biodivers Conserv (2009) 18:829 846 833 Table 1 List of species preyed by feral cats (Felis silvestris catus) in the Canary Islands Preys Distribution BGR IUCN SRDB CNEA CEAC References Mammals Atelerix algirus T, C, F, L INT LR/lc Medina et al. (2008) Atlantoxerus getulus F INT LC Medina et al. (2008) Rattus spp. P, G, H, T, C, F, L INT LR/lc Nogales and Medina (1996) Mus musculus domesticus P, G, H, T, C, F, L INT LR/lc Nogales and Medina (1996) Oryctolagus cuniculus P, G, H, T, C, F, L INT LR/lc Nogales and Medina (1996) Birds Non-passerines Bulweria bulwerii P, G, H, T, C, F, L NAT LC EN LC VU Ardura and Calabuig (1993) Calonectris diomedea borealis P, G, H, T, C, F, L NAT LC VU LC LC Nogales et al. (1988) Puffinus assimilis P, G, H, T, C, F, L NAT LC EN VU VU Ardura and Calabuig (1993) Hydrobates pelagicus G, H, T, C, F, L NAT LC VU LC LC Ardura and Calabuig (1993) Alectoris rufa C INT LC Santana et al. (1986) Columba livia P, G, H, T, C, F, L NAT LC Nogales et al. 1988; Medina and Nogales (1993) Passerines Calandrella rufescens rufescens T NAT LC CR LC LC Lorenzo et al. (2002) Anthus berthelotii berthelotii P, G, H, T, C, F, L END LC LC LC Nogales et al. (1988); Medina et al. (2006) Erithacus rubecula superbus T, C END LC LC LC Rodríguez et al. (1996) Saxicola dacotiae F END EN EN VU VU Illera and Díaz (2006) Turdus merula cabrerae P, G, H, T, C NAT LC Medina et al. (2006) Sylvia conspicillata orbitalis P, G, H, T, C, F, L NAT LC LC LC Medina et al. (2006) Sylvia melanocephala leucogastra P, G, H, T, C, F, L END LC LC LC Medina et al. (2006) Phylloscopus canariensis P, G, H, T, C END LC LC LC Nogales et al. (1988); Medina et al. (2006)

834 Biodivers Conserv (2009) 18:829 846 Table 1 continued Preys Distribution BGR IUCN SRDB CNEA CEAC References Parus caeruleus teneriffae G, T, C END LC LC LC Rodríguez and Moreno (1993) Pyrrhocorax pyrrhocorax barbarus P NAT LC EN LC VU Medina et al. (2006) Fringilla coelebs palmae P END LC EN LC LC Medina et al. (2006) Fringilla teydea polatzeki C END LC CR EN EN Rodríguez and Moreno (1993) Serinus canarius P, G, H, T, C, F, L NAT LC Santana et al. (1986); Nogales et al. (1988) Reptiles Gekkonidae Tarentola angustimentalis F, L END LC LC Nogales et al. (1990); Medina et al. (2008) Tarentola boettgeri H, C END LC LC Santana et al. (1986); Nogales et al. (1988) Tarentola delalandii P, T END LC LC Nogales et al. (1990); Medina et al. (2006) Lacertidae Gallotia atlantica mahoratae F END LC LC Medina et al. (2008) Gallotia caesaris caesaris H END LC LC Nogales et al. (1988) Gallotia caesaris gomerae G END LC LC Nogales and Medina (1996) Gallotia galloti galloti T END LC LC Medina and Nogales (1993) Gallotia galloti palmae P END LC LC Medina et al. (2006) Gallotia gomerana G END CR CR Nogales et al. (2001) Gallotia intermedia T END CR CR EN EN Hernández et al. (2000) Gallotia simonyi machadoi H END CR CR EN EN Rodríguez-Domínguez et al. (1998); García-Márquez et al. (1997) Gallotia stehlini C END LC LC LC LC Santana et al. (1986) Scincidae Chalcides sexlineatus C END LC LC LC LC Santana et al. (1986)

Biodivers Conserv (2009) 18:829 846 835 Table 1 continued Preys Distribution BGR IUCN SRDB CNEA CEAC References Chalcides viridanus coeruleopunctatus G, H END LC LC Nogales et al. (1988) Chalcides viridanus viridanus T END LC LC Medina and Nogales (1993) Invertebrates Mollusca Gastropoda Theba geminata P, G, H, T, C, F, L END Medina et al. (2008) Rumia decollata P, G, H, T, C, F, L NAT Medina et al. (2008) Malacostraca Isopoda Armadillidium vulgare P, G, H, T, C, F INT Medina and García (2007) Diplopoda Julida Blaniulus guttulatus P, G, T NAT Medina and García (2007) Chilopoda Scolopendra valida P, G, T, C NAT Santana et al. (1986); Medina and García (2007) Hexapoda Odonata Anax imperator P, G, H, T, C, F, L NAT LC Medina et al. (2008) Orthoptera Acrididae Dericorys lobata C, F, L NAT Medina et al. (2008) Gryllidae Gryllomorpha longicauda P, H, T NAT Medina and García (2007) Gryllus bimaculatus P, G, H, T, C, F, L INT Santana et al. (1986)

836 Biodivers Conserv (2009) 18:829 846 Table 1 continued Preys Distribution BGR IUCN SRDB CNEA CEAC References Tettigonidae Decticus albifroms P, H, G, T, C NAT Medina and García (2007) Dermaptera Anisolabididae Anisolabis maxima P, T, C, F NAT Nogales et al. (1988) Coleoptera Carabidae Laemostenus complanatus P, H, T, C, F, L INT Medina and García (2007) Curculionidae Brachyderes rugatus P, H, T, C, L END Santana et al. (1986) Coniocleonus exocoriatus P, H, T, C, F, L NAT Medina et al. (2008) Conorhynchus conicirostris P, H, T, C, F, L NAT Medina et al. (2008) Herpisticus calvus C, F, L END Medina et al. (2008) Scarabeidae Oryctes prolixus P, H, G, T, C END Nogales et al. (1988); Medina and García (2007) Pachydema fuscipennis P, G, T, C, F END Medina and García (2007) Phyllognatus excavatus P, T, C, F, L NAT Medina et al. (2008) Tropinota squalida canariensis P, G, H, T, C, F, L END Medina and García (2007) Staphylinidae Ocypus olens P, G, H, T, C, F, L NAT Medina and García (2007) Tenebrionidae Hegeter glaber P END Medina and García (2007) Hegeter tristis P, H, G, T, F, L NAT Medina and García (2007) Paivaea hispida C, F, L END Medina et al. (2008) Pimelia laevigata costipennis H END Nogales et al. (1988)

Biodivers Conserv (2009) 18:829 846 837 Table 1 continued Preys Distribution BGR IUCN SRDB CNEA CEAC References Pimelia laevigata laevigata P END Medina and García (2007) Cerambycidae Arhopalus pinetorum P, H, G, T NAT Medina and García (2007) Deroplia albida P, G, T, C, F, L END Medina and García (2007) Lepidoptera Gracillariidae Phyllocnistis canariensis P, G, T END Medina and García (2007) Sphingidae Hyles tithymali tithymali P, G, H, T, C, F, L END Medina and García (2007) Hymenoptera Anthophoridae Anthophora alluaudi P, G, H, T, C, F, L END Medina and García (2007) Melecta curvispina P, G, T, C END Medina and García (2007) BRG, biogeographic range; IUCN, IUCN Red List of Threatened Species categories; SRDB, Spanish Red Data Books; CNEA, Spanish endangered species list; CEAC, Canarian endangered species list; INT, introduced species; END, endemic species; NAT, native species; P, La Palma; G, La Gomera; H, El Hierro; T, Tenerife; C, Gran Canaria; F, Fuerteventura; L, Lanzarote; LR, lower risk; LC, least concern; VU, vulnerable; CR, critically endangered; EN, endangered

838 Biodivers Conserv (2009) 18:829 846 (García-Márquez et al. 1997; Rodríguez-Domínguez et al. 1998), Gallotia intermedia from Tenerife (Hernández et al. 2000) and Gallotia gomerana from La Gomera (Nogales et al. 2001). The rest of species included in the IUCN Red List are being considered species of least concern or they had not been deemed as threatened (see Table 1). At national level, 12 species affected by feral cats appeared in the Spanish Red Data Books (Pleguezuelos et al. 2004; Madroño et al. 2005): the three giant lizards, previously commented, and nine bird species (Calonectris diomedea borealis and H. pelagicus as vulnerable, C. r. rufescens and F. t. polatzeki as critically endangered, and B. bulwerii, P. assimilis, S. dacotiae, F. c. palmae and Pyrrhocorax pyrrhocorax barbarus as endangered). However, these species are not equally considered in the Spanish and the Canarian Endangered Species Acts (see Table 1). For example, while two of the three threatened giant lizards (G. simonyi and G. intermedia) are considered endangered in both Endangered Species Acts (Gobierno de Canarias 2003; Martín et al. 2005b), the other one (G. gomerana) is not currently included even though this species probably is one of the most threatened lizard of the world (Valido et al. 2000). Nevertheless, the Canary Government has recently proposed its incorporation into the Spanish Endangered Species Act (Martín et al. 2005b). Other species preyed on by feral cats in the Canaries, such as B. bulwerii, P. assimilis, C. diomedea, H. pelagicus, C. rufescens, P. pyrrhocorax, and F. c. palmae, are also included in the Spanish Red Data Book of Birds (Madroño et al. 2005) as endangered or critically endangered but they are considered as least concern species in both official endangered species lists, except P. assimilis which has been considered as vulnerable in the Canary Islands (Table 1). Consequently, we believe that it is important to secure the legal status of these species in order to promote an effectively protection of their endangered populations (Taylor 2000). Although feral cats have been globally associated with declines or extinctions of the largest number of native and endemic species on islands (Dickman 1996; Courchamp et al. 2003), it is very difficult to conclude that there is a directly relationship between introduced species and declining indigenous species because of other complicating factors (Towns et al. 2006). Some evidence of feral cat impact on native species included, among others, predation, restoring endangered species after eradication, comparing reproductive success before and after control, comparison between cat-inhabited and catfree islands, and local extinctions (Arnaud et al. 1993; Hodges and Nagata 2001; Mitchell et al. 2002; Edwards et al. 2004; Phillips et al. 2005; Rodríguez et al. 2006). Dietary studies could be a poor indicator of impacts on populations, particularly when the prey is rare or affected intermittently (Towns et al. 2006). Moreover, the number of prey eaten by a predator is not necessarily the same as the number killed by it, which is important in assessing the ecological role of feral cats (Patronek 1998). Nevertheless, on islands where a high number of endemic and endangered species are found, studies on diet or feeding ecology of feral cats had been performed considering the predation as potentially important evidence of their incidence on native species (Nogales et al. 1990; Seabrook 1990; Arnaud et al. 1993; Chapuis et al. 1994; Donlan et al. 2000; Winter and Wallace 2006). Moreover, the study of feral cats diet could be considered as the first step to interpret the impact of this predator on prey populations (Paltridge et al. 1997). According with this, we consider that reviewing the results obtained in studies of feral cats diet constitute an interesting tool to predict detrimental effects in the conservation of the endangered species on island environments, even when the presence of one predator only has been considered sufficient to induce the extinction of the endemic prey (Courchamp et al. 1999).

Biodivers Conserv (2009) 18:829 846 839 Feral cat control in the Canary Islands Feral cats are directly responsible for a large percentage of global extinctions, particularly on islands worldwide, and for this reason they have been removed from at least 48 islands around the world (Nogales et al. 2004). Taking into account that feral cats constitute a major threat to endemic reptile species on islands (Iverson 1978; Arnaud et al. 1993) and considering the negative impact of feral cats in the particular case of the endangered Canarian giant lizards (García-Márquez et al. 1997; Hernández et al. 2000; Nogales et al. 2001), several management controls of feral cat populations had been implemented in those areas where giant lizards are still extant (Table 2). While in El Hierro Island feral cats were removed from the areas where a reintroduction program of G. simonyi was performed (Silva and Mateo 2003), the management control of feral cats in La Gomera Island provoked a beneficial effect on the wild population of G. gomerana (Mateo 2001). Lastly, in the case of G. intermedia the control was mainly carried out in order to prevent the proliferation of domestic cats in the giant lizard distribution areas (Rando 2005). In addition to cat control a permanent fence was placed in order to prevent the entrance of cats into the population of this endangered species (Rando 2005). In the case of the Canarian endangered bird species, several control programmes have been performed in specific areas in order to minimize the effect of feral cat on their populations (Table 2). For example, a population control was carried out in Gran Canaria and Tenerife to minimize their effects on an endangered population of F. t. polatzeki and C. r. rufescens, respectively (Rafael Riera, pers. com.; Lorenzo et al. 2002). On other hand two successfully feral cat eradications have been carried out in two small islets (Alegranza and Lobos) where some important seabird colonies have been seriously affected by this predator (Ardura and Calabuig 1993; Rodríguez-Luengo and Calabuig 1993; Martín et al. 2002a, b). The most noteworthy programs of feral cats eradication had been carried out on islands where a high number of endemic bird species are found (Nogales et al. 2004). Although these short term conservation actions are important to reduce the impact of feral cats on these endangered species, we consider that these efforts should be maintained at long term time scale, and regularly during each year, in order to minimize their conservation concerns. As occur worldwide, in the Canary Islands people (about 2 million persons) love cats because they are considered as a beneficial animal helping humans controlling plagues such as rats and mice. Moreover, in some islands of the archipelago, endemic species such as lizards (Gallotia spp.) or pigeons (Columba bollii and C. junoniae) are considered as plagues due to their damage to farm and crops. Probably, for this reason cats had not been previously considered as a conservation concern in this archipelago. Moreover, a common practice in several islands is to release kittens in the wild when the owners do not want more cats at home. These facts could be considered as a very important limitation to develop control programmes in addition to the great variability of habitats and the abrupt topography of the main islands. General consideration on hyperpredation and mesopredation release In general, the relationship between population size of feral cats and damage on their endangered populations could be overestimated, ignoring temporal and spatial variation in environmental conditions and variation in the density of other species (Edwards et al. 2004). In the case of the Canary Islands the presence of other introduced mammals, such as rats or mice, together with human disturbance (habitat destruction and fragmentation), could compound feral cats effects on endemic and endangered species. So, the presence of

840 Biodivers Conserv (2009) 18:829 846 Table 2 Resume of the control programmes of feral cats (Felis silvestris catus) carried out in the Canary Islands Island Is. surface (km 2 ) Control area (km 2 ) Habitat Control period Methods Cats removed Other introduced predators Main species affected References Alegranza 10.2 10.2 XS May 1998 Live traps 1 Mus domesticus Bulweria bulwerii Calonectris diomedea Puffinus assimilis Pelagodroma marina Hydrobates pelagicus Oceanodroma castro Lobos 4.4 4.4 XS Sep 1992 19 23 May 1997 21 29 Aug 2002 Tenerife Los Rodeos Live traps, poison 2034.4 &1 Grassland 2001 2002 Live traps 54 Mus domesticus Rattus rattus Rattus norvegicus Atelerix algirus Tenerife 2034.4 0.25 XS Nov 04 Feb 05 Live traps 35 Mus domesticus Teno a Rattus norvegicus Rattus rattus Gran Canaria Inagua Gran Canaria Tamadaba 1560.1 39.2 PF 1996 1997 1999 2002 Live traps 17 51 6 0 3 Mus domesticus Bulweria bulwerii Calonectris diomedea Puffinus assimilis Pelagodroma marina Hydrobates pelagicus Oceanodroma castro Mus domesticus Rattus rattus Rattus norvegicus Atelerix algirus 1560.1 &1 PF Nov Dec 2002 Live traps 3 Mus domesticus Rattus rattus Rattus norvegicus Atelerix algirus Martín et al. (2002a) Ardura and Calabuig (1993) M. González, pers. com. Martín et al. (2002b) Callandrella rufescens Lorenzo et al. (2002) Gallotia intermedia Rando (2005) Fringilla teydea Rodríguez et al. (1997) Rodríguez et al. (2003) Fringilla teydea Rodríguez et al. (2003)

Biodivers Conserv (2009) 18:829 846 841 Table 2 continued Island Is. surface (km 2 ) Control area (km 2 ) Habitat Control period Methods Cats removed Other introduced predators Main species affected References Canaria Maspalomas 1560.1 &5 TF, Dunes Jul Oct 2008 Live traps 30 Mus domesticus Rattus rattus Rattus norvegicus Atelerix algirus Gran Canaria 1560.1 300 PF Jul Oct 2008 Live traps 85 Mus domesticus Rattus rattus Rattus norvegicus Atelerix algirus El Hierro 268.7 &40 XS, TF 2001 2005 Live traps 275 Mus domesticus Rattus rattus La Gomera a 369.8 &1 XS 17 30 Sep 1999 2000 2001 Live traps 7 58 Mus domesticus Rattus rattus Charadrius alexandrinus R. Riera, pers. com. Fringilla teydea R. Riera, pers. com. Gallotia simonyi Rodríguez-Domínguez et al. (2007) Gallotia gomerana Illera (1999) Mateo (2001) XS, Xerophytic Shrub; TF, Termophyle Forest; PF, Pine Forest These management controls were mainly carried out on domestic or stray cat populations due to their close distribution to the giant lizard populations a

842 Biodivers Conserv (2009) 18:829 846 a controlled population of cats might be, at least temporarily, more beneficial to their endemic prey than its eradication, as occur in the cases on many islands where rodents have also been introduced (Courchamp et al. 1999; Rayner et al. 2007). On islands, where introduced mammals constituted the main prey of feral cats (Fitzgerald 1988; Nogales and Medina 1996), this predator could reduce the rodent populations at low levels and could outweigh the damage done to the endemic prey species. For example in the laurel forests of the Canary Islands there are not evidence of predation by feral cats upon endemic pigeons (Columba bolli and C. junoniae) (Nogales and Medina 1996) but by rats (R. rattus) which prey on eggs, chicks, juveniles and adults of these two endemic pigeons (Hernández et al. 1999; Martín et al. 2000). Rats constituted the main prey item of feral cats in this ecosystem (Nogales et al. 2006), showing the indirect role that cats might play in preserving native fauna through reduction of rat predation pressure on endemic pigeons. For this reason the management of feral cat populations should be developed taking into account the mesopredator release effect, where the elimination of feral cat populations from such ecosystems could lead to a more severe negative impact on the endemic species, as a result of expansion of rodent population once their predators are removed (Courchamp et al. 1999). This important aspect has been considered when the feral cats control campaigns have been carried out in the cases of G. intermedia (Rando 2005) and C. r. rufescens (Lorenzo et al. 2002). In both cases other mammals predators such as rats, mice or Hedgehogs (Atelerix algirus) which could be affected their endangered populations were also removed. So, taking into account the predictions made in the different models presented (Courchamp et al. 1999, 2000) and the results obtained in the different studies (i.e., Rayner et al. 2007), we consider that control programmes of the introduced predators on islands must be performed simultaneously to the mesopredators and introduced prey control in order to avoid undesirables and irreversible effects on endemic species. Conclusions In the Canary Islands it is necessary to enforce management controls of feral cat populations on those areas where highly endangered species populations have been seriously affected by feral cats, such as the distribution areas of giant lizards in Tenerife, La Gomera and El Hierro islands. Nevertheless, it is important to take into account the presence of other introduced predators and prey such as rats, mice or rabbits in order to avoid problems derived from the hyperpredation process and mesopredator release effect as have been previously mentioned. Finally, in the Canary Islands, as well as in other island ecosystems, priority management requirements for endangered species must include the prevention of the introduced mammals spread (Nogales et al. 2004), removing introduced predator from endangered species distribution areas, researching their ecological role for eradication programmes (Courchamp et al. 2003; Taylor 2000), and the development of education campaigns for people about the problematic of pets release into natural ecosystems. Acknowledgments We thank all the co-authors who participated with us in the partial contributions carried out on the study of feral cat diet in the Canary Islands, without their basic information this review had not been possible. Manuel González-Acebes, Aurelio Martín, Juan Carlos Illera, Juan Carlos Rando, Rafael Riera and Miguel Ángel Rodríguez-Domínguez provided useful information about feral cat control programmes performed in the Canary Islands. Thanks to Rafael Riera who support data from Gran Canaria Island control programmes financed by the Cabildo Insular de Gran Canaria and the Canary Government. This contribution has been carried out during the project GL2004-04884-C02-01/BOS financed by the Spanish Ministry of Science and the European Union.

Biodivers Conserv (2009) 18:829 846 843 References Ardura E, Calabuig P (1993) Depredación de pequeños procelariformes y control de gatos asilvestrados en el islote de Lobos. Unpublished report to the Unidad de Fauna, Viceconsejería de Medio Ambiente, Consejería de Política Territorial, Gobierno de Canarias, Las Palmas de Gran Canaria Arnaud G, Rodríguez-Moreno A, Ortega A, Álvarez S (1993) Predation by cats on the unique endemic lizard of Socorro Island (Urosaurus auriculatus), Revillagigedo, Mexico. Ohio J Sci 93:101 104 Chapuis JL, Boussès P, Barnaud G (1994) Alien mammals, impact and management in the French sub- Antarctic islands. Biol Conserv 67:97 104. doi:10.1016/0006-3207(94)90353-0 Courchamp F, Langlais M, Sugihara G (1999) Cats protecting birds: modelling the mesopredator release effect. J Anim Ecol 68:282 292. doi:10.1046/j.1365-2656.1999.00285.x Courchamp F, Langlais M, Sugihara G (2000) Rabbits killing birds: modelling the hyperpredation process. J Anim Ecol 69:154 167 Courchamp F, Chapuis JL, Pascal M (2003) Mammal invaders on islands: impact, control and control impact. Biol Rev Camb Philos Soc 78:347 383. doi:10.1017/s1464793102006061 Dickman CR (1996) Overview of the impacts of feral cats on Australian native fauna. Australian Nature Conservation Agency and Institute of Wildlife Research, University of Sydney, Canberra and Sydney Donlan DJ, Tershy BR, Keitt BS, Wood B, Sánchez JA, Weinstein A, Croll DA, Aguilar JL (2000) Island conservation action in northwest Mexico. In: Browne DH, Chaney H, Mitchell K (eds) Proceedings of the fifth California Islands symposium. Santa Barbara Museum of Natural History, Santa Barbara, California, pp 330 338 Driscoll CA, Menotti-Raymond M, Roca AL, Hupe K, Johnson WE, Geffen E, Harley EH, Delibes M, Pontier D, Kitchener AC, Yamaguchi N, O Brien SJ, Macdonald DW (2007) The near eastern origin of cat domestication. Science 317:519 523. doi:10.1126/science.1139518 Edwards GP, Pople AR, Saalfeld K, Caley P (2004) Introduced mammals in Australian rangelands: future threats and the role of monitoring programmes in management strategies. Aust Ecol 29:40 50. doi: 10.1111/j.1442-9993.2004.01361.x Fitzgerald BM (1988) Diet of domestic cats and their impact on prey populations. In: Turner DG, Bateson P (eds) The domestic cat: the biology of its behaviour. Cambridge University Press, Cambridge, pp 144 Fitzgerald BM, Turner BM (2000) Hunting behaviour of domestic cats and their impact on prey populations. In: Turner DC, Bateson P (eds) The domestic cat: the biology of its behaviour, 2nd edn. Cambridge University Press, Cambridge, pp 151 175 García-Márquez M, Caetano A, Bello I, López-Jurado LF, Mateo JA (1997) Ecología del gato cimarrón en el ecosistema termófilo de El Hierro (Islas Canarias) y su impacto sobre el lagarto gigante (Gallotia simonyi). Monogr Herpetol 4:207 222 Gobierno de Canarias (2003) Fauna y flora de Canarias en el Catálogo Nacional de Especies Amenazadas. Consejería de Política Territorial y Medio Ambiente, Gobierno de Canarias Gorman ML (1979) Island ecology. Chapman and Hall, London Hernández MA, Martín A, Nogales M (1999) Breeding success and predation on artificial nests of the endemic pigeons Bolle s laurel pigeon Columba bollii and white-tailed laurel pigeon C. junoniae in the laurel forest of Tenerife (Canary Islands). Ibis 141:52 59. doi:10.1111/j.1474-919x.1999.tb04262.x Hernández E, Nogales M, Martín A (2000) Discovery of a new lizard in the Canary Islands, with a multivariate analysis of Gallotia (Reptilia: Lacertidae). Herpetologica 56:63 76 Hodges CSN, Nagata RJ Sr (2001) Effects of predator control on the survival and breeding success of the endangered Hawaiian Dark-rumped Petrel. Stud Avian Biol 22:308 318 Illera JC (1999) Intensificación de los muestreos de captura de la nueva especie de lagarto gigante encontrado en la isla de La Gomera (Gallotia aff. simonyi); trampeo de gato cimarrón en Quiebracanillas y prospección de nuevas zonas en las inmediaciones de dicho enclave. Unpublished report. Consejería de Medio Ambiente y Política Territorial, Gobierno de Canarias Illera JC, Díaz M (2006) Reproduction in an endemic bird of a semiarid island: a food-mediated process. J Avian Biol 37:447 456. doi:10.1111/j.2006.0908-8857.03676.x IUCN (2007) 2007 IUCN Red List of threatened species. Available from http://www.iucnredlist.org. Cited 9 Jan 2008 Iverson JB (1978) The impact of feral cats and dogs on populations of the West Indian rock iguana, Cyclura carinata. Biol Conserv 14:63 73. doi:10.1016/0006-3207(78)90006-x Jehl JR Jr, Parks KC (1983) Replacements of landbird species on Socorro Island, Mexico. Auk 100: 551 559 Lever C (1994) Naturalized animals. T and AD Poyser Natural History, London

844 Biodivers Conserv (2009) 18:829 846 Lorenzo JA, Rodríguez B, Izquierdo C, de León L, Puerta N, Alonso J (2002) Seguimiento de la terrera marismeña y control de los factores de amenaza en Tenerife. SEO/BirdLife, La Laguna Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world s worst invasive alien species: a selection from the Global Invasive Species Database. SSC, IUCN, Gland Mac Arthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton Madroño A, González C, Atienza JC (eds) (2005) Libro Rojo de las Aves de España. Dirección General para la Biodiversidad-SEO/BirdLife, Madrid Martín A, Delgado G, Nogales M, Quilis V, Trujillo O, Hernández E, Santana F (1989) Premières données sur la nidification du Puffin des Anglais (Puffinus puffinus), du Pétrel-frégate (Pelagodroma marina) et de la Sterne de Dougall (Sterna dougallii) aux Îles Canaries. L Oiseau et R. FO 59:73 83 Martín A, Hernández MA, Lorenzo JA, Nogales M, González C (2000) Las palomas endémicas de Canarias. Gobierno de Canarias and SEO/Birdlife, Santa Cruz de Tenerife Martín A, Nogales M, Alonso J, Rodríguez B, De León L, Izquierdo C, Martín M, Marrero P, Puerta N, Cazorla J, Rodríguez B, López M, Martínez J, Pérez D, Ginovés J, González E (2002a) Restauración de los Islotes y del Risco de Famara (Lanzarote). Departamento de Biología Animal (Zoología), Universidad de La Laguna, La Laguna Martín A, Lorenzo JA, Rodríguez B, Nogales M (2002b) Erradicación de gatos asilvestrados en el islote de Lobos. Departamento de Biología Animal (Zoología), Universidad de La Laguna, La Laguna Martín JL, Marrero M, Zurita N, Arechavaleta M, Izquierdo I (2005a) Biodiversidad en gráficas. Especies silvestres de las Islas Canarias. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, Santa Cruz de Tenerife Martín JL, Fajardo S, Cabrera MA, Arechavaleta M, Aguiar A, Martín S, Naranjo M (2005b) Evaluación 2004 de especies amenazadas de Canarias. Consejería de Medio Ambiente y Ordenación Territorial, Gobierno de Canarias, Santa Cruz de Tenerife Mateo JA (2001) Lagarto Gigante de La Gomera. Annual report Gobierno de Canarias Medina FM, García R (2007) Predation of insects by feral cats (Felis silvestris catus L., 1758) on an oceanic island (La Palma, Canary Islands). J Insect Conserv 11:203 207. doi:10.1007/s10841-006-9036-7 Medina FM, Nogales M (1993) Dieta del gato cimarrón(felis catus L.) en el piso basal del Macizo de Teno (Noroeste de Tenerife). Donana Acta Vert 20:291 297 Medina FM, Nogales M (2007) Habitat use of feral cats in the main environments of an Atlantic Island (La Palma, Canary Islands). Folia Zool (Brno) 56:277 283 Medina FM, García R, Nogales M (2006) Feeding ecology of feral cats on a heterogeneous subtropical oceanic island (La Palma, Canarian Archipelago). Acta Theriol (Warsz) 51:75 83 Medina FM, López-Darias M, Nogales M, García R (2008) Food habits of feral cats (Felis silvestris f. catus, L. 1758) in insular semiarid environments (Fuerteventura, Canary Islands). Wildl Res 35:162 169. doi: 10.1071/WR07108 Mellink E (1992) The status of Neotoma anthonyi (Rodentia, Muridae, Cricetinae) of Todos Santos Islands Baja California Mexico. Bull South Calif Acad Sci 91:137 140 Mitchell N, Haeffner R, Veer V, Fulford-Gardner M, Clerveaux W, Veitch CR, Mitchell G (2002) Cat eradication and the restoration of endangered iguanas (Cyclura carinata) on Long Cay, Caicos Bank, Turks and Caicos Islands, British West Indies. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. SSC, IUCN, Gland, pp 206 212 Nogales M, Medina FM (1996) A review of the diet of feral domestic cats (Felis silvestris f. catus) on the Canary Islands, with new data from the laurel forest of La Gomera. Z Saugetierkunde 61:1 6 Nogales M, Martín A, Delgado G, Emmerson K (1988) Food sprectrum of the feral cat (Felis catus L.,1758) in the juniper woodland on El Hierro (Canary Islands). Bonn Zool Beitr 39:1 6 Nogales M, Abdola M, Alonso C, Quilis V (1990) Premiêres données sur l alimentation du chat haret (Felis catus L., 1758) du Parc National du Teide. Ténérife (Iles Canaries). Mammalia 54:189 196 Nogales M, Rodríguez JL, Delgado G, Quilis V, Trujillo O (1992) The diet of feral cats (Felis catus) on Alegranza Island (North of Lanzarote, Canary Islands). Folia Zool (Brno) 4:209 212 Nogales M, Rando JC, Valido A, Martín A (2001) Discovery of a living giant lizard, genus Gallotia (Reptilia: Lacertidae), from La Gomera, Canary Islands. Herpetologica 57:169 179 Nogales M, Martín A, Tershy BR, Donlan CJ, Veitch D, Puerta N, Wood B, Alonso J (2004) A review of feral cat eradication on islands. Conserv Biol 18:310 319. doi:10.1111/j.1523-1739.2004.00442.x Nogales M, Rodríguez-Luengo JL, Marrero P (2006) Ecological effects and distribution of invasive nonnative mammals on the Canary Islands. Mammal Rev 36:49 65. doi:10.1111/j.1365-2907. 2006.00077.x Paltridge R, Gibson D, Edwards G (1997) Diet of the feral cat (Felis catus) in Central Australia. Wildl Res 24:67 76. doi:10.1071/wr96023

Biodivers Conserv (2009) 18:829 846 845 Patronek GJ (1998) Free-roaming and feral cats-their impact on wildlife and human beings. JAVMA 212:218 226 Phillips RB, Cooke BD, Campbell K, Carrion V, Marquez C, Snell HL (2005) Eradicating feral cats to protect Galapagos Land Iguanas: methods and strategies. Pac Conserv Biol 11:257 267 Pleguezuelos JM, Márquez R, Lizana M (eds) (2004) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española, Madrid Randi E, Ragni B (1991) Genetic variability and biochemical systematics of domestic and wild cat populations (Felis silvestris: Felidae). J Mammal 72:79 88. doi:10.2307/1381981 Rando JC (2003) Protagonistas de una catástrofe silenciosa: los vertebrados extintos de Canarias. Indiferente 14:4 15 Rando JC (2005) Actuaciones para el control de las colonias de gatos (Felis catus) del Barranco de Masca. Unpublished report to the Cabildo Insular de Tenerife, Santa Cruz de Tenerife Rayner MJ, Hauber ME, Imber MJ, Stamp RK, Clout MN (2007) Spatial heterogeneity of mesopredator release within an oceanic island system. Proc Natl Acad Sci USA 104:20862 20865. doi: 10.1073/pnas.0707414105 Rodríguez F, Moreno AC (1993) Programa de conservación del pinzón azul de Gran Canaria (Fringilla teydea polatzeki Hartert, 1905) 1991 1993 I poblaciones, reproducción, características del hábitat e incidencia de depredadores. Viceconsejería de Medio Ambiente, Gobierno de Canarias, Las Palmas de Gran Canaria Rodríguez F, Moreno AC, González M, Riera R (1996) Programa de conservación del pinzón azul de Gran Canaria Fringilla teydea polatzeki Hartert, 1905 Memoria 1995. Viceconsejería de Medio Ambiente, Gobierno de Canarias, Las Palmas de Gran Canaria Rodríguez F, Moreno AC, González M (1997) Acciones para la conservación del pinzón azul de Gran Canaria Memoria final. Viceconsejería de Medio Ambiente, Gobierno de Canarias, Las Palmas de Gran Canaria Rodríguez F, Moreno AC, González M, Riera R, Santana G (2003) Conservación del pinzón azul de Gran Canaria: Proyecto No LIFE98NAT/5354 Informe final. Viceconsejería de Medio Ambiente, Gobierno de Canarias, Las Palmas de Gran Canaria Rodríguez C, Torres R, Drummond H (2006) Eradicating introduced mammals from a forested tropical island. Biol Conserv 130:98 105. doi:10.1016/j.biocon.2005.12.005 Rodríguez-Domínguez MA, Coello JJ, Castillo C (1998) First data on the predation of Felis catus L.,1758 on Gallotia simonyi machadoi López-Jurado, 1989 in El Hierro, Canary Islands (Sauria, Lacertidae). Vieraea 26:169 170 Rodríguez-Domínguez MA, González-Ortega C, Mesa-Ávila G, Lucía-Bohórquez M, Molina-Borja M (2007) Plan de recuperación del lagarto gigante de El Hierro: estado actual y perspectivas futuras. El Indiferente 19:30 41 Rodríguez-Luengo JL, Calabuig P (1993) Programa de control de gatos asilvestrados en la isla de Lobos. Viceconsejería de Medio Ambiente, Gobierno de Canarias, La Laguna Santana F, Martín A, Nogales M (1986) Datos sobre la alimentación del gato cimarrón (Felis catus Linnaeus, 1758) en los montes de Pajonales, Ojeda e Inagua (Gran Canaria). Vieraea 16:113 117 Seabrook W (1990) The impact of the feral cat (Felis catus) on the native fauna of Aldabra Atoll, Seychelles. Rev Ecol (Terre Vie) 45:135 145 Serpell JA (2000) Domestication and history of the cat. In: Turner DC, Bateson P (eds) The domestic cat: the biology and its behaviour. Cambridge University Press, Cambridge, pp 179 192 Silva JL, Mateo JA (2003) El Lagarto Gigante de El Hierro: reflexiones sobre su recuperación. Medio Ambiente Canarias 25:13 16 Taylor GA (2000) Action plan for seabird conservation in New Zealand. Part A: threatened seabirds. Department of Conservation, Biodiversity Recovery Unit, Wellington Tershy BR, Donlan DJ, Keitt BS, Croll DA, Sánchez JA, Wood B, Hermosillo MA, Howald GR, Biavaschi N (2002) Island conservation in north-west Mexico: a conservation model integrating research, education and exotic mammal eradication. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. World Conservation Union, Gland, pp 293 300 Towns DR, Atkinson EAE, Daugherty DH (2006) Have the harmful effects of introduced rats on islands been exaggerated? Biol Inv 8:863 891. doi:10.1007/s10530-005-0421-z Valido A, Rando JC, Nogales M, Martín A (2000) Fossil lizard found alive in the Canary Islands. Oryx 34:75 76 Veitch CR (2001) The eradication of feral cats (Felis catus) from Little Barrier Island, New Zealand. N Z J Zool 28:1 12 Vigne JD, Guilaine J, Debue K, Haye L, Gérard P (2004) Early taming of the cat in Cyprus. Science 304:259

846 Biodivers Conserv (2009) 18:829 846 Whittaker RJ, Fernández-Palacios JM (2007) Island biogeography: ecology, evolution and conservation. Oxford University Press, Oxford Winter L, Wallace GE (2006) Impacts of feral and free-ranging cats on bird species of conservation concern: a five-state review of New York, New Jersey, Florida, California, and Hawaii. American Bird Conservancy, The Plains, VA