Bringing Science Back to the Conservation of the Iberian Lynx

ALEJANDRO RODRÍGUEZ,∗§ JAVIER CALZADA,† ELOY REVILLA,∗ JOSE´ VICENTE LO´ PEZ- BAO,‡ AND FRANCISCO PALOMARES∗ ∗ Department of Conservation Biology, Estacioń Biolo´gica de Donãna—CSIC, Ame´rico Vespucio s/n, Isla de la Cartuja, 41092 Sevilla, Spain †Departamento de Biolog´ıa Ambiental y Salud Pu´blica, Universidad de Huelva, Avda Fuerzas Armadas s/n, 21071 Huelva, Spain ‡Grimso¨ Wildlife Research Station, Department of Ecology, Swedish University of Agricultural Sciences—SLU, SE-73091 Riddarhyttan, Sweden

Palomares et al. (2011) highlighted 4 factors ported by Rodr´ıguez and Delibes (1992, 2002). Simo associated with the reduced effectiveness of efforts to ń et al. suggest that Rodr´ıguez and Delibes (1992, conserve Iberian lynx (Lynx pardinus) during the 2002) over- estimated the area occupied by lynx in last 25 years: conservation measures have not been the past. Simoń et al. argue these retrospective applied over large extents, few resources have been estimates were obtained from indirect methods, but dedicated to scientific monitoring of the effectiveness they ignore that the estimates were derived from a of conservation actions, conservation efforts were systematic field survey in which sampling effort was implemented discontinuously, and practitioners have consistent throughout the potential range of lynx and, limited confidence in scientific knowledge. The therefore, results were spatially unbi- ased (Rodr authors of Simoń et al. (2012) are members of the ´ıguez & Delibes 2002). In contrast, estimates of the largest team currently managing Iberian lynx, and they past distribution of Iberian lynx presented by Gil- S contend that the trends in lynx abundance reported ánchez and McCain (2011) relied mostly on in Palomares et al. (2011) overlook that there have been specimens deposited in zoological collections and, substantial increases in the number of lynx over the last hence, mainly reflect the areas scientists visited to decade, that managed areas are large enough to sus- collect samples of Iberian lynx. tain the species, that monitoring suggests Habitat management before natural or assisted management has increased lynx abundance, and that recol- onization is rarely applied to large areas. Simoń management, especially under a consecutive set of et al. recognize that most conservation efforts were projects funded by the European Union (LIFE) for the concen- trated in the 1832 km2 already occupied by conservation of Iberian lynx in Andalusia, is long- the Iberian lynx. We acknowledge that focusing habitat lasting. We disagree and argue that available evidence, management on occupied areas may increase the including that summarized by Simoń et al., supports number of reproductive females and, therefore, the our position. probability of long-term population persistence Simoń et al. report that the areas occupied by the (Palomares et al. 2011). As carrying capacity is 2 remaining populations of Iberian lynx and total approached, improving habitat quality on the edges of abundance of lynx increased by a factor of 2.5 lynx habitat in Sierra Morena or in the interior of the from 2002 to 2011. This increase does not affect the Donãna National Park would allow more dispersers evidence of long-term decline of Iberian lynx. to establish territories and breed, and fewer Palomares et al. (2011) estimated that the 2 current dispersers would move into adjacent low-quality 2 Iberian lynx populations occupied 19,800 km in habitat. There have been recent reintroductions in 1955. On the basis of this estimate, range loss in 2005 eastern Sierra Morena (Simoń et al.), and the European was 93.9%, whereas on the basis of data provided by Union LIFE conservation project, which commenced at Simoń et al., estimated range loss in 2010 was the end of 2011 (see Table 1 in Simoń et al.), aims to 96.4%. The recent expansion of lynx range (410 km2 fund conservation of Iberian lynx in 5 regions across from 2002 to 2010 [Simoń et al.]) would be the Iberian peninsula. Concentrating available remarkable if the past lynx range had been smaller resources to increase the area than previously re-

§Address for correspondence: email [email protected] Paper submitted October 27, 2012; revised manuscript accepted March 21, 2012.

.x of breeding habitat, or creating a new, large area of will reliably increase rabbit abundance elsewhere. lynx habitat, could be equally or more efficient than Nevertheless, the short-term assessment of effects of creating a large number of comparatively small and supplementary feeding on lynx behavior and isolated habitat patches. In particular, habitat demography by Lo´pez-Bao and co-workers management over relatively large areas has not been undertaken outside Andalusia. Because mean time to extinction increases quickly as carrying capacity increases (Palomares et al. 2011), a small number of relatively large lynx populations may be the best strategy (McCarthy et al. 2005), but we believe before multiple reintroduction attempts are embarked on, models and data should be used to determine the optimal number of populations to be established or maintained. The link between the inefficiency of Iberian lynx conservation measures and a lack of scientific monitoring was identified more than a decade ago (Rodr´ıguez et al. 2000). Simoń et al. argue that the Iberian lynx LIFE project team conducts scientific monitoring because the team in- cludes scientists who evaluate management actions, the conservation programs are reviewed by an external scientific panel, and the populations of lynx and their prey (the European rabbit [Oryctolagus cuniculus]) are monitored with standardized techniques. Monitoring should examine the extent to which the change one observes in a given behavioral or demographic parameter in the Iberian lynx can be attributed to one or more conservation actions. Estimating abundances of lynx and rabbits (Garrote et al. 2011; Gil-Sánchez et al. 2011) with methods such as camera trapping and counting rabbits in lin- ear transects, respectively, will allow data collected over time to be compared. But use of such methods does not directly address the more important question of whether changes in lynx abundance are the result of previous management efforts. Simoń et al. seem to assume that increases in abundance or number of populations of lynx or rabbits are mostly a consequence of management, but such relations may be correlative. For example, during the last decade many lynx emigrated from and started to breed outside Donãna National Park. In other words, natural coloniza- tion occurred first, breeding females were discovered later (because areas outside the park were not monitored until lynx were occasionally detected), and management was eventually applied to colonized areas. We question whether such expansion could be attributed to management. Likewise Simoń et al. report significant increases in rabbit abundance in some areas but, as pointed out by Palomares et al. (2011), it is unclear whether these increases were a response to management or largely to extrinsic factors (e.g., higher resistance to viral dis- eases or reduced mortality attributed to other predators), whether some measures were more efficient than others, or whether particular measures is a recent example of monitoring of the efficiency of although food availability increased, general lynx a specific conservation measure, perhaps the only scarcity in the region resulted in lit- tle immigration and case in the history of Iberian lynx conservation. In this reduced opportunities for dispersers to establish case, lynx responses (Lo´pez-Bao et al. 2008, 2010) territories in managed habitat (Lo´pez-Bao et al. and some of the mechanisms involved in their 2010). responses (Lo´pez-Bao et al. Table 1 in Simoń et al. shows the reliance of con- 2009, 2011) were servation of Iberian lynx on external funding. investigated. Although regional governments execute Simoń et al. conclude that efforts to conserve environmental policies, including species the Iberian lynx have been consistent because conservation, on average European Union funds made funding for conservation projects has been up 68.3% of the total cost of the 27 projects (93%) continuous since 1994. However, the actions reported on in Simoń et al. (LIFE Nature implemented, the locations where they were applied, 2012). Dependence on EU funding makes continuity and funding of each action in each area often varied of conservation action even less likely, especially from one 5-year LIFE project to the next. As a result, during pe- riods of economic uncertainty. Moreover, it is difficult to assess the efficacy of a given regional recov- ery plans were made mandatory by a conservation action (Lo´pez-Bao et al. 2010). Also, 1990 law, but it took 13–21 years to approve the actions that are expected to be beneficial only in plans in 3 autonomous regions, and 2 other regions the long term were interrupted before they could have not approved them yet. Limited funding and have a measurable effect. For example, a plan to marked slowness in establishing specific regulations increase the carrying capacity of the core area of suggest there is room for improvement in the Donãna National Park for breeding lynx was resolution with which regional governments act initiated in 2004 under the auspices of the Iberian regarding Iberian lynx conservation. lynx LIFE project team. Although preliminary results Until 2008 managers and professional researchers were promising in terms of retention of breeding co- operated, and scientific knowledge guided adults (Lo´pez-Bao et al. 2008, 2010), actions such as management, especially in the Donãna population of supplementary feeding of lynx or rabbit restock- ing lynx. Since 2002 scientists who are members of the in predator-proof enclosures were discontinued 3 Iberian lynx LIFE project team have documented years later. Three years may be too short a period to variation in lynx and rabbit abundances, which is ex- pect definitive results or even to generate necessary but not sufficient to evaluate implemented sufficient data on which to base decisions about the management actions on the basis of sound science. effectiveness of a specific plan. For example, Data from scientific monitoring of

Conservation Biology Volume 26, No. 4, 2012 specific conservation actions will inform decisions asymmetries in the use of supplementary food by the endangered on how to efficiently apply the relatively scarce Iberian lynx (Lynx pardinus). Public Library of Science ONE economic resources available to maintain Iberian lynx 4 in areas they currently occupy and to increase the DOI:10.1371/journal.pone.0007610. Lo´pez-Bao, J. V., F. Palomares, A. Rodr´ıguez, and M. Delibes. probability of recol- onization of currently unoccupied 2010. Ef- fects of food supplementation on home range size, areas. reproductive suc- cess, productivity and recruitment in a small population of Iberian lynx. Animal Conservation 13:35–42. Lo´pez-Bao, J. V., F. Palomares, A. Rodr´ıguez, and P. Ferreras. Literature Cited 2011. Intraspecific interference influences the use of prey hotspots. Oikos Garrote, G., et al. 2011. Estimation of the Iberian lynx (Lynx 120:1489–1496. pardinus) population in the Donãna area, SW Spain, using McCarthy, M. A., C. J. Thompson, and H. P. Possingham. 2005. capture-recapture analysis of camera-trapping data. European The- ory for designing nature reserves for single species. The Journal of Wildlife Re- search 57:355–362. American Naturalist 165:250–257. Gil-Sánchez, J. M., and E. B. McCain. 2011. Former range and Palomares, F., A. Rodr´ıguez, E. Revilla, J. V. Lo´pez-Bao, and J. decline of the Iberian lynx (Lynx pardinus) reconstructed Calzada. using verified records. Journal of Mammalogy 92:1081–1090. 2011. Assessment of the conservation efforts to prevent Gil-Sánchez, J. M., et al. 2011. The use of camera trapping for extinction of the Iberian lynx. Conservation Biology 25:4–8. estimating Iberian lynx (Lynx pardinus) home ranges. Rodr´ıguez, A., and M. Delibes. 1992. Current range and status of European Journal of Wildlife Research 57:1203–1211. the Iberian lynx Felis pardina Temminck, 1824 in Spain. LIFE Nature. 2012. Online project database. Environment Biological Conservation 61:189–196. Directorate, General European Commission (DG ENV.E.3), Rodr´ıguez, A., and M. Delibes. 2002. Internal structure and patterns Brussels, Bel- gium. Available from of contraction in the geographic range of the Iberian lynx. h ttp://ec.europa.eu/environment/life/project/ Projects/index.cfm Ecography (accessed March 2012). 25:314–328. Lo´pez-Bao, J. V., A. Rodr´ıguez, and F. Palomares. 2008. Rodr´ıguez, A., P. Ferreras, and M. Delibes. 2000. On recent actions Behavioural response of a trophic specialist, the Iberian lynx, undertaken for the conservation of the Iberian lynx. Pages 85– to supplementary food: patterns of food use and implications 87 in Report of the group of experts on conservation of large for conservation. Biological Conservation 141:1857–1867. carni- vores. Document T-PVS (2000) 33. Council of Europe, Lo´pez-Bao, J. V., A. Rodr´ıguez, and F. Palomares. 2009. Strasbourg, France. Competitive Simoń M. A., et al. 2012. Reverse of the decline of the endangered Iberian lynx. Conservation Biology 26:731–736. Conservation Biology Volume 26, No. 4, 2012