Assessment of the Conservation Efforts to Prevent Extinction of the Iberian Lynx FRANCISCO PALOMARES,∗ ‡ ALEJANDRO RODRÍGUEZ,∗ ELOY REVILLA,∗ JOSÉ VICENTE LÓPEZ-BAO,∗ AND JAVIER CALZADA† ∗ Department of Conservation Biology, Estación Biológica de Doñana (CSIC), Américo Vespucio s/n, Isla de la Cartuja, 41092 Sevilla, Spain †Departamento de Biologı́a Ambiental y Salud Pública, Universidad de Huelva, Av Fuerzas Armadas s/n, 21071 Huelva, Spain Abstract: The Iberian lynx ( Lynx pardinus) may be the first charismatic felid to become extinct in a high-income country, despite decades of study and much data that show extinction is highly probable. The International Union for Conservation of Nature categorizes it as critically endangered; about 200 freeranging individuals remain in two populations in southern Spain. Conservation measures aimed at averting extirpation have been extensively undertaken with 4 of the former 10 Iberian lynx populations recorded 25 years ago. Two of the four populations have been extirpated. The number of individuals in the third population have declined by 83%, and in the fourth the probability of extirpation has increased from 34% to 95%. Major drivers of the pending extinction are the small areas to which conservation measures have been applied; lack of incorporation of evidence-based conservation, scientific monitoring, and adaptive management into conservation efforts; a lack of continuity in recovery efforts, and distrust by conservation agencies of scientific information. In contrast to situations in which conservation and economic objectives conflict, in the case of the Iberian lynx all stakeholders desire the species to be conserved. Keywords: evidence-based conservation, extinction probability, Iberian lynx, Lynx pardinus, management practice Evaluación de los Esfuerzos de Conservación para Prevenir la Extinción del Lince Ibérico Resumen: El lince ibérico ( Lynx pardinus) puede ser el primer felino carismático que se extinga en un paı́s desarrollado, a pesar de décadas de estudio y muchos datos que muestran que su extinción es altamente probable. La Unión Internacional para la Conservación de la Naturaleza lo clasifica como en peligro crı́tico; quedan alrededor de 200 individuos en libertad en dos poblaciones en el sur de España. Se han tomado medidas de conservación extensivas dirigidas a evitar la desaparición de 4 de las 10 poblaciones de lince ibérico registradas hace 25 añ os. Dos de esas 4 poblaciones han desaparecido. El nú mero de individuos en una tercera población ha disminuido un 83% y, en la cuarta, la probabilidad de extinción ha incrementado del 34% al 95%. Las principales causas de la situación actual son el pequeño tamañ o de las áreas en las que se han aplicado las medidas de conservación; la falta de incorporación de medidas basadas en la evidencias, de seguimiento cientı́fico y de manejo adaptativo en los esfuerzos de conservación; la falta de continuidad en los esfuerzos de recuperación y la desconfianza de las agencias de conservación en la información cientı́fica. En contraste con situaciones donde los objetivos económicos y de conservación entran en conflicto, en el caso del lince ibérico todas las partes interesadas desean que la especie sea conservada. Palabras Clave: conservación basada en evidencias, lince Ibérico, Lynx pardinus, manejo adaptativo, probabilidad de extinción ‡email ffpaloma@ebd.csic.es 4 Introduction In 1986 the International Union for Conservation of Nature (IUCN) listed the Iberian lynx (Lynx pardinus) as endangered (von Arx & Breitenmoser-Würsten 2008), and 10 years later it was the only species in category 1 (highest global and regional concern) of the global ranking of felid vulnerability developed by Nowell and Jackson (1996). The species’ small geographic range and specific resource requirements contributed to its assignment to this threat category. Sixteen years later it was recategorized as critically endangered (von Arx & BreitenmoserWürsten 2008), which means the probability of extinction in the wild is extremely high. Around 1980 only 1100 individuals remained in 10 isolated populations on the Iberian Peninsula (Spain and Portugal) (Rodrı́guez & Delibes 1992; Castro & Palma 1996). These data prompted development of a profusion of conservation plans by regional, national, and European government and nongovernmental organizations. Eight plans have been published since 1980. The first was the Management Plan for the Iberian Lynx in Doñana National Park (the most studied population occurs in the park). Despite widespread social concern and the development of these plans, the Iberian lynx still has a high probability of extinction. In 16 years (1985–2001) the size of its geographic range and breeding area have decreased; abundance of breeding females and of all individuals decreased by 86–93% (Calzada et al. 2007); and 8 of the 10 populations were extirpated (Calzada et al. 2007; Sarmento et al. 2009) (Fig. 1). Currently, about 200 free-ranging individuals remain in southern Spain. They comprise two populations that are 240 km apart, Sierra Morena and Doñana. Trends in the Remaining Iberian Lynx Populations The size of the Doñana population has been approximately 50 over the last 25 years (Fig. 1). In Doñana, lynx range over 2000 km2 and form a metapopulation with source–sink dynamics (Gaona et al. 1998). Persistence of the meta population depends on the evolution of source populations (Gaona et al. 1998; Revilla & Wiegand 2008) that occur within the Doñana National Park boundaries (550 km2 ). Between 1985 and 2005, the number of breeding territories inside the park decreased from 11 from 1985 through 1992, to 9 in 1997, and to 5 in 2005. This decline in breeding territories in the park increased the probability of the species’ extirpation in 100 years from 34%, to 46%, and to 95%, respectively (Gaona et al. 1998; Revilla & Wiegand 2008) (Fig. 2). The probability of extirpartion of the Doñana metapopulation increased to 98% in the spring of 2007, when an outbreak of feline leukemia killed three of the four adult males remaining in Doñana National Park. Six infected lynx (four males and two females) were removed from the area and held in captivity (Meli et al. 2009) (Fig. 2). The extirpation of the Doñana metapopulation might be prevented if the equivalent of 10 new territories could be established in the park and 14 lynx could be translocated over 5 years. Such an increase in number of potential territories and individuals would decrease extirpation probability to <10% and would significantly increase the persistence time of the Doñana population (Fig. 2). Lynx translocations from Sierra Morena would also help increase genetic diversity of the Doñana population, which is 33% lower than that of the Sierra Morena population (Johnson et al. 2004), and forestall inbreeding depression. Available data do not allow quantification of the probability of the extirpation of the Sierra Morena population, but between 1985 and 2005 this population exhibited a pattern of range contraction similar to other populations that have already been extirpated (Fig. 1). In spite of this, the Sierra Morena population may be able to withstand extraction of four cubs and four juveniles per year (Palomares et al. 2002b). Conservation Efforts Extensive conservation measures aimed at averting extirpation have been undertaken for 4 of the former 10 Iberian lynx populations. The success of these efforts has been negligible, however. The Malcata (Portugal) and Toledo Mountains populations were extirpated; between 1985 and 2005, the number of individuals in the Sierra Morena population declined by 83%; and the probability of extirpation of the Doñana population increased from 34% to 95%. The most conservation efforts have been aimed at the Doñana and Malcata populations. In the Doñana National Park since 1986 more than 19 lynx conservation projects have been implemented. The average duration for 12 of them was 4 years (there is no information on duration for the seven remaining projects). Budgets for 10 projects for which data are available collectively amounted to over €11 million. Furthermore, other long-term management projects in the Doñana region, not explicitly aimed at Iberian lynx, included measures meant to improve the quality of lynx habitat and to reduce mortality on roads. Since 2002, two European Union conservation projects (i.e., LIFE projects) contributed €31 million to the conservation of the two remaining lynx populations. Because private foundations and nongovernmental organizations also implemented many local conservation projects, we estimate that no less than €60 million were spent in Spain over the last 30 years on conservation of the Iberian lynx. Areas in Malcata were protected in 1981 with the specific aim of preserving an Iberian lynx population, and the bulk of the resources for lynx conservation in Portugal was allocated for this project. Nevertheless, lynx Figure 1. Area of occupancy of the six largest Iberian lynx populations (outlined key) from 1955 to 2005 and estimated population size (number of individuals) of the two remaining populations, Doñana and Sierra Morena, in 1985 and 2005. The estimates of area of occupancy between 1955 and 1985 were taken from Rodrı́guez and Delibes (2002). After 1985 data is from Palomares et al. (1991), Ferreras (2001), Rodrı́guez (2002), and Román et al. (2006) for the Doñana population; from Palomares et al. (2002a), Guzmán et al. (2004), and Consejerı́a de Medio Ambiente (2006) for the Sierra Morena population; and from Ceia et al. (1998) and Sarmento et al. (2009) who reported the near extinction of the Iberian lynx in Portugal. Population size estimates in 1985 and 2005 are from Rodrı́guez and Delibes (1992), Román et al. (2006), and Consejerı́a de Medio Ambiente (2006). were extirpated in Malcata around 1997 (Sarmento et al. 2009). Reasons for the Limited Success of Conservation Efforts In spite of listing, comprehensive scientific knowledge (Ferreras et al. 2010), and remarkable conservation efforts, Iberian lynx continue to decline. We believe there are four synergistic factors in the limited success of lynx conservation that may apply to other endangered species. First, conservation measures have not been applied over large extents. Adult Iberian lynx need 5–15 km2 of territory (Ferreras et al. 2010), which means a population of 50 breeding females requires about 500 km2 of high-quality habitat. Small population size and associated stochastic processes likely drove extirpation of many Iberian lynx populations (Rodrı́guez & Delibes 2003). To maximize the probability of survival over 40 years, populations require areas >500 km2 , an area in which observed extirpation frequencies are zero. For populations occupying areas of 250–500 km2 and <100 km2 observed extirpation frequencies are 0.63 and 0.75, respectively (Rodrı́guez & Delibes 2003). Thus, conservation measures applied over small areas are unlikely to be effective. In general, extensive improvements to habitat quality and habitat-restoration projects are not simple or inexpensive (e.g., Wilcove & Chen 1998). For the Iberian lynx, interventions to improve habitat quality include extensive removal of forestry plantations, clearing of scrubland, increasing the abundance of prey by building warrens and translocating rabbits (Oryctolagus cunniculus), and construction of underpasses to decrease mortality of lynx on roads (Ferreras et al. 2010). With the exception mentioned above for Doñana, the government allocation for conservation of lynx has been generally insufficient and applied only to several small disparate areas. Therefore, if sufficient funds cannot be raised, concentrating money and effort in selected large areas might be accomplished through collaborative planning among stakeholders, such as regional and national governments and nongovernmental organizations. Second, few resources have been dedicated to scientific monitoring of the effectiveness of conservation actions. Consequently, although many different Figure 2. Doñana National Park population of Iberian lynx (a) probability of extirpation in 100 years (grey bars) and mean time to extirpation (black bars) and (b) population size (number of individuals) (grey bars), population size coefficient of variation (dots), and average number of resident females (black bars) under different conservation strategies: A, lynx population in 2007 after a feline leukemia outbreak; B, translocation of individuals to account for the lynx that died of feline leukemia; C, increase in carrying capacity of the main source area by 10 territories; D, scenarios B+C; E, as in scenario D plus translocation of 10 lynx into the main source population. Details of the simulation model used to generate results shown in these figures are in Revilla and Wiegand (2008). conservation tools have been tried, alone or in combination, little has been learned about the reasons for their efficiency or failure. Moreover, the absence of scientific monitoring of individual projects has precluded changes in goals and practices under the principles of adaptive management or evidence-based conservation (Sutherland et al. 2004). Although the necessity of scientific monitoring has been emphasized in conservation plans for the Iberian lynx (particularly in those redacted during the last 10 years), it has rarely been carried out in practice. The lack of monitoring is due to allocation of all the limited funds available to implementation of conservation measures, despite considerable uncertainty of their efficacy. As a result, some conservation measures have been applied for over 20 years without measurable success. For example, rabbits are the main prey of Iberian lynx, and recovery of Iberian lynx depends in part on recovery of rabbit populations. Considerable effort has been put into increasing the abundance of rabbits in Doñana National Park. Over the last 20 years approximately 30,000 rabbits were translocated to the park, but there has been no noticeable increase in the abundance of rabbits (Fernández 2005), and it is unknown whether local or temporal increases in the abundance of rabbits are attributable to the translocations. We believe no effective method to increase rabbit abundances has been developed because rabbit populations have not been monitored adequately. Some monitoring of rabbits has been conducted, but these efforts often lacked scientific rigor. Critical and objective assessments through systematic monitoring of conservation actions should be performed, preferably by people who were not involved in plan development. Third, often management plans were developed with the input of elected officials, whose tenures were short (<5 years), and this contributed to a lack of continuity in recovery efforts. Furthermore, most management plans do not include adaptive management components. Thus, instead of revising a plan to address changes in the situation new management plans have to be developed, which slows the conservation process. Fourth, practitioners working on Iberian lynx recovery have limited confidence in scientific knowledge. Sometimes scientific advice has been taken into consideration when it was too late to act on that advice. Reintroduction of lynx to areas where they had been extirpated was recommended 10 years ago (Delibes et al. 2000), but the first reintroduction began at the end of 2009. In addition, specific studies were conducted to inform reintroductions. Recommendations derived from these studies followed IUCN guidelines (Rodrı́guez et al. 2003) and provided details on how many free-ranging individuals could be extracted from donor populations to minimize negative effects (Palomares et al. 2002b). The results of updated population viability analyses that incorporated many different management scenarios and outcomes within an adaptive-management context have been available (in the form of internal reports and presentations at numerous venues) since 2006. None of the reintroduction recommendations or PVA results have been incorporated into existing management plans. Conservation efforts may fail simply because information transfer among scientists, managers, and politicians is imperfect or because detailed conservation planning is lacking (Groves et al. 2002). Nevertheless, this has not been the case with Iberian lynx conservation. Most scientific information on the species is available in diverse and accessible peer-reviewed journals (Ferreras et al. 2010), scientists have participated in most meetings organized by local, regional, or national management agencies, and researchers have been actively involved in the preparation of management plans. 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