The Iberian Lynx Lynx Pardinus Conservation Breeding Program A

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The Iberian lynx Lynx pardinus Conservation Breeding Program A. VARGAS1, I. SA´ NCHEZ2, F. MARTI´NEZ1, A. RIVAS1, J. A. GODOY3, E. ROLDA´ N4, M. A. SIMO´ N5, R. SERRA6, MaJ. PE´ REZ7, C. ENSEN˜ AT8, M. DELIBES3, M. AYMERICH9, 10 11 A. SLIWA & U. BREITENMOSER 1Centro de Cr´ıa de Lince Ibe´rico El Acebuche, Parque Nacional de Don˜ ana, Huelva, Spain, 2Zoobota´ nico de Jerez, Ca´ diz, Spain, 3Don˜ ana Biological Station, CSIC, Sevilla, Spain, 4National Museum of Natural Science, CSIC, Madrid, Spain, 5Environmental Council, Andalusian Government, Jae´ n, Spain, 6Investigac¸a˜ o Veterina´ ria Independente, Lisbon, Portugal, 7Centro de Cr´ıa en Cautividad de Lince Ibe´rico La Olivilla, Jaen, Spain, 8Parc Zoolo´ gic, Barcelona, Spain, 9Direccio´ n General para la Biodiversidad, Ministerio de Medio Ambiente, Madrid, Spain, 10Cologne Zoo, Cologne 50735, Germany, and 11IUCN Cat Specialist Group, Institute of Veterinary Virology, University of Bern, Bern, Switzerland E-mail: [email protected]

The Iberian Lynx Conservation Breeding Program fol- INTRODUCTION lows a multidisciplinary approach, integrated within the National Strategy for the Conservation of the Iberian lynx, which is carried out in cooperation with national, Iberian lynx Lynx pardinus wild populations regional and international institutions. The main goals of have undergone a constant regression through- the ex situ conservation programme are to: (1) maintain a out the last century. The decline has been genetically and demographically managed captive popu- especially abrupt in the last 20 years, with more lation; (2) create new Iberian lynx Lynx pardinus free- ranging populations through re-introduction. To achieve than an 80% reduction, mostly owing to the the first goal, the Conservation Breeding Program aims to dramatic decline of wild rabbit Oryctolagus maintain 85% of the genetic diversity presently found in cuniculus populations, the lynx’s prey base. the wild for the next 30 years. This requires developing According to the last census (Guzmań et al., and maintaining 60–70 Iberian lynx as breeding stock. 2002), o200 Iberian lynx (only half of them Growth projections indicate that the ex situ programme should achieve such a population target by the year 2010. considered to be adults with reproductive po- Once this goal is reached, re-introduction efforts could tential) survive in nature. The last two remnant begin. Thus, current ex situ efforts focus on producing populations, Don˜ ana and Sierra Morena, are psychologically and physically sound captive-born indi- located in Andalusia, southern Spain. This viduals. To achieve this goal, we use management and research techniques that rely on multidisciplinary input dramatic population decline has brought the and knowledge generated on species’ life history, beha- species to what is known as an ‘extinction viour, nutrition, veterinary and health aspects, genetics, vortex’. The small size of both populations reproductive physiology, endocrinology and ecology. makes them highly vulnerable to stochastic Particularly important is adapting our husbandry schemes events, such as natural disasters (e.g. forest based on research data to promote natural behaviours in captivity (hunting, territoriality, social interactions) and a fires, flooding), disease outbreaks, genetic and stress-free environment that is conducive to natural demographic problems, etc., that could com- reproduction. pletely wipe out a remnant population within a very short period of time (Delibes et al., 2000). Key-words: adaptive management; applied research; conservation breeding; ex situ; genetics; husbandry; The species is listed as Critically Endangered Iberian lynx; outreach; re-introduction; reproductive by The World Conservation Union (IUCN, physiology; veterinary science. 2006).

Owing to the precarious situation of the make pairing recommendations based on Iberian lynx in the wild, conservation mea- genetic distance between breeders, etc. One sures need to be implemented effectively and of our goals is to minimize the use of efficiently, integrating efforts and working potentially invasive methods while simulta- tools (Heredia et al., 1999; MIMAM, 1999). neously enhancing the trust between the Iberian lynx conservation could be conceived lynxes and their keepers to assist in securing as a puzzle whose pieces should fit together information on animal body mass and gesta- adequately. Primary efforts should be direc- tional status. Over the past 3 years, eight ted towards in situ conservation, which in- pregnancies have resulted in the birth of 19 cludes (1) maintaining and expanding offspring, of which 11 survive to date (Vargas remnant populations, monitoring, managing et al., 2007). While describing various orga- prey (wild Rabbit) populations, protecting nizational aspects of the Iberian lynx Con- and restoring habitat, promoting agreements servation Breeding Program, this paper will with land owners, minimizing non-natural also emphasize how results from multidisci- causes of mortality and connecting, from a plinary life-science research can be integrated genetic standpoint, the two remnant popula- into an adaptive management approach to tions, and (2) preparing habitat for creating help recover the world’s most threatened felid new free-ranging populations. Another piece species. of the puzzle is ex situ conservation, which includes, among other activities, captive THE IBERIAN LYNX EX SITU breeding, preparing animals for release, re- CONSERVATION PROGRAM search in different areas, management of a Biological Resource Bank (BRB), genetic The Iberian Lynx Ex Situ Conservation Breed- management of all lynx populations (wild ing Program follows a multidisciplinary ap- and captive) as a single metapopulation, as proach, integrated within the National well as training staff, education and outreach Strategy for the Conservation of the Iberian efforts (Vargas, Sańchez et al., 2005). lynx, officially endorsed by the Spanish Current Iberian lynx conservation-breed- National Commission for the Protection of ing efforts focus on producing psychologi- Nature. National, regional and international cally and physically sound captive-born institutions collaborate with the Program, individuals. For this purpose, we use manage- which is currently implemented through a ment and research techniques that rely on ‘multilateral commission’ that involves the multidisciplinary input and knowledge, gen- central governments of Spain and Portugal, erated on the life history of the species, together with the autonomous governments of behaviour, nutrition, veterinary and health Andalusia, Extremadura and Castilla-La Man- aspects, genetics, reproductive physiology, cha, Spain. Portugal, where no Iberian lynx endocrinology and ecology. Particularly im- populations were detected during the last portant is adapting our husbandry schemes 2002–2003 census, has developed its own ex based on research data to promote natural situ conservation action plan, prepared in behaviours in captivity (hunting, territoriality, coordination with the Iberian lynx captive social interactions) and a stress-free environ- breeding committee (Serra et al., 2005; see ment that is conducive to natural reproduc- also Vargas, 2006). tion. Some relevant research areas include: The main goals of the Iberian Lynx Con- determining faecal hormone profiles for adult servation Breeding Program are twofold: (1) and subadult lynxes, studying reproductive to maintain a genetically and demographi- behaviour and cub development, determining cally managed captive population that serves the reproductive health of < and , breeders, as a ‘safety net’ for the species and (2) to help developing a non-invasive pregnancy test, establish new Iberian lynx free-ranging po- establishing sound biosecurity and biomedi- pulations through re-introduction pro- cal protocols, genotyping all founders and grammes. Because the extraction of large

number of lynxes from the last two remnant populations could compromise their viability, the most viable way to create new populations is through the re-introduction of individuals born in captivity. To achieve the latter goal, the Conservation Breeding Program must be integrated with in situ measures, such as the conservation and restoration of potential Iberian lynx habitat in areas of historical presence of the species (Andalusia, Castilla- La Mancha, Extremadura and Portugal) The Iberian Lynx Program encompasses management and applied research strategies in the following six areas. 1. Genetic and demographic management of the captive population The best genetic management of threatened captive populations is achieved through rapid population growth until the established number of individuals required to maintain genetic variability for the species in question is reached (Lacy, 1994). Afterwards, population size should be stabilized. In order to implement this approach, the production of new individuals must be planned properly to meet both re- introduction and breeding programme needs, because the latter will gradually require the Plate 1. Iberian lynx Lynx pardinus , and cub which replacement of older individuals past their are part of the Iberian Lynx Conservation Breeding reproductive prime. Genetic and population Program in Spain. Iberian Lynx Ex Situ Conservation management must be accompanied by proper Program, Ministry of the Environment, Madrid, and Environmental Counsel of Andalusia (MMA-CMA). husbandry, which involves stimulating natural behaviours in captive-born individuals from early developmental periods in order to improve their potential for survival in the 5 year period. Wild-born founders should be wild (Plate 1). selected from large litters (of three or more Based on recommendations provided by siblings), because the extraction of such in- the IUCN Conservation Breeding Specialist dividuals will have a lower impact in the wild Group, in collaboration with the Iberian lynx population (Lacy & Vargas, 2004). The main- in situ conservation managers, the actual tenance of genetic diversity over 30 years situation of this species will allow for the will, therefore, require a group of 60 (30.30) conservation of 85% of the current genetic breeding animals (comprising the original variability for a period of 30 years (Lacy & founders plus individuals born in the Con- Vargas, 2004; Godoy, 2006). Captive popula- servation Breeding Program). As a basic tions that maintain o85% genetic variability strategy for maintaining genetic variability, it are considered to be dangerously inbred. is important to achieve rapid population In order to achieve the established genetic growth over the ﬁrst 10 years of the Program, goals, four wild-born cubs/juveniles (foun- until it reaches its ‘capacity phase’, estab- ders) must be incorporated into the Breeding lished at 60 breeding individuals. Efforts Program each year for 5 years consecutively. should also be made to ensure equal repre- Thus, 20 cubs/juveniles are needed within a sentation of founders, which should all

provide a similar number of offspring to the Center has developed a standard operational- Program. procedures manual that details the various 2. Captive husbandry Captive husbandry is protocols that are applied to its breeding based on multidisciplinary input from a vari- population (see Vargas, Mart´ınez et al., ety of animal-care fields, such as nutrition, 2005). Detailed protocols based on experi- behaviour, genetics, physiology and veterin- ences at the ‘pilot facilities’ will help smooth ary medicine, together with the systematic the way towards unified practices across ex use of the scientific method. Over the past situ lynx breeding centres as new centres two decades, a great deal of knowledge and open. experience has been gained in the manage- 3. Health and veterinary aspects The health ment of wild felids in captivity. The Associa- considerations involved in captive breeding, re- tion of Zoos and Aquariums Felid Taxon introduction and translocation programmes are a Advisory Group has compiled a Husbandry source of great concern to conservation biologists. Manual for Small Felids containing useful For instance, mycoplasmosis in Mohave desert information on, for example, health, repro- tortoises Xerobates agassizi (Jacobson, 1991), duction, nutrition and facilities (Mellen & equine encephalitis in Whooping cranes Grus Wildt, 1998). Many European zoos have americana (Dein et al., 1986), diaphragmatic broad-ranging experience in breeding wild hernias in Golden lion tamarins Leontopithecus cats in general and lynxes in particular. These rosalia (Bush et al., 1993) and herpes virus in a documents and experiences have been and large list of captive-bred avian species (Viggers continue to be a very useful reference to the et al., 1993) are just a few examples of health Iberian Lynx Captive Breeding Program problems associated with small, threatened popula- (Vargas et al., 2006). tions. There have been various cases in which One of the Program’s key husbandry chal- captive-bred animals re-introduced into the wild lenges is to strike a balance between fostering have transmitted infectious diseases to wild popu- natural behaviours in captivity (hunting, ter- lations; for example, tuberculosis in reintro- ritoriality, social interactions, etc.) and creat- duced Arabian oryx Oryx leucoryx (Viggers ing a stress-free environment where animals et al., 1993). Also, wild-caught individuals are more prone to mate. In order to obtain have occasionally infected captive populations important information about the animals with potentially lethal diseases [e.g. canine (such as their body mass or determining distemper in Black-footed ferrets Mustela ni- whether or not the ,, are pregnant), certain gripes (Williams et al., 1988)]. It is generally training techniques are being used. Some of felt that most of these conservation pro- these include obtaining regular body-mass grammes were lacking sufficient information measurements by encouraging the lynx to on: (1) disease distribution and risk in captive step onto a measuring scale. Such techniques populations; (2) disease incidence, distribution are designed to avoid using invasive meth- and risk in wild populations; (3) quarantine ods, which would stress the animals, and they systems to prevent disease transmission; (4) a also serve as a way to strengthen the bond system to track and detect pathogens ade- between the animals and their keepers. quately. The animals’ behaviour is also being care- Because relatively little is known about the fully observed by a round-the-clock video- diseases affecting lynx, actions to improve surveillance system, which provides a great our knowledge of the main diseases affecting deal of information on the species that could the species are imperative. The Iberian Lynx not be learned easily through observations in Conservation Breeding Program has a Veter- the wild. Based on the experience acquired at inary Advisory Team dedicated to diverse the ‘El Acebuche’ Center and at the Jerez aspects of veterinary and research manage- Zoo, together with information obtained from ment, as well as protocol development. To programmes established at European and tackle the understanding of the various dis- American zoos, the El Acebuche Breeding eases that potentially affect the species, the

Program’s main lines of action involve the searched at the Institute for Zoo and Wildlife establishment of preventive disease protocols Research in Berlin (Jewgenow et al., 2006). for the captive populations, and research on The non-invasive techniques described above general veterinary science (Mart´ınez, 2006). provide a great deal of information, while Projects are now under way to determine minimizing the disturbance of the animals the incidence and prevalence of infectious under study. Assessment of reproductive pathogens in captive and wild lynx popula- health by trans-rectal ultrasound has also been tions (Meli et al., 2006; Milla´ n, 2006), deter- applied to study physiological changes in < mination of normal vs pathological blood and , Iberian lynx (F. Goeritz, unpubl. data). values (Munõz et al., 2006; Pastor et al., This knowledge has been essential to assess 2006) and research on potential renal disfunc- the reproductive soundness of the captive tion (Jimeńez et al., 2006). The results of population of Iberian lynx and it is regularly research, protocol developments and standar- used to make management decisions regard- dization efforts, coupled with dissemination ing the pairings of captive animals. and sharing of knowledge and experience In order to assist breeding and maintaining among veterinarians working in the pro- gene diversity, the Iberian Lynx Ex Situ gramme, are all contributing to more consis- Program collaborates with the maintenance tent diagnosis and treatment. For further of a Biological Resources Bank for conserva- information, see http://www.lynxexsitu.es/ tion of biomaterial gathered from wild and aaveterinaros/aaveterinarios.htm captive Iberian lynx populations (Leoń et al., 4. Reproductive physiology Reproductive 2006; Roldań et al., 2006). In order to physiology studies and associated technolo- conserve the maximum possible genetic di- gies increase the success rate of any captive- versity, samples of < and , gametes, as well breeding programme and are important in as different cells or tissues, are being kept. helping with the conservation of wild felids The conservation of gametes allows us to in captivity. Reproductive technologies are extend future options without the limitations available for three major purposes: (1) asses- of space, or the risk of disease transmission. sing fertility and monitoring reproductive Also, the cryopreservation of gametes and status; (2) assisting in breeding and mainte- embryos allows for the opportunity of nance of gene diversity; (3) learning more prolonging the possibilities of reproduction about reproductive mechanisms of the Criti- for individual animals after their death. The cally Endangered Iberian lynx. preservation of somatic cells (or undifferen- An important outcome of Iberian lynx tiated germ cells) could give individuals who reproductive physiology studies is the devel- have died before reaching sexual maturity a opment of non-invasive techniques that aid in reproductive opportunity, or extend the repro- captive population management. Over the ductive potential of other individuals. past 2 years, work carried out to define Iberian The Iberian lynx BRB is presently being lynx < and , hormonal profiles has helped us maintained at two locations: the National gain a clearer perspective on the length of Museum of Natural Sciences in Madrid breeding periods, and the potential use of (Roldań et al., 2006) and the Miguel Hernań- hormonal metabolites in faeces as a non- dez University in Elche, Alicante (Leoń et al., invasive gestation predictor (Jewgenow 2006). Although the Museum of Natural et al., 2006; Pelican et al., 2006; see also Sciences specializes principally in reproductive Schwarzenberger, 2007). While faecal hor- samples and the University MH specializes in mones do not seem to be the best diagnostic multi-potential somatic cells, both banks pre- tool, they have proven to be extremely useful serve tissue, blood, serum and other biological to understand better the year-round reproduc- materials. The storage of these samples means tive activity of < and , Iberian lynx. Another that materials will be available for future gestation diagnostic technique, based on ana- analysis whenever needed, which is a valuable lyses of relaxin in urine, is now being re- resource for potential retrospective studies.

5. Re-introduction As mentioned above, joyed by conservation-breeding programmes the two current small populations of free- is their ability to gain public attention, parti- ranging Iberian lynxes are highly vulnerable. cularly if the animal in question is charismatic Thus, it is imperative to create, as soon as and attractive to the broader public. The possible, new wild populations (while simul- Iberian lynx is one such case and raising taneously increasing numbers in the existing public awareness of the need for habitat ones). conservation to guarantee survival of the Before any re-introduction/translocation, a species in the wild is one of the Program’s detailed viability study is required (see IUCN primary objectives. It is important to empha- Guidelines for Re-introductions: IUCN, size that breeding and keeping lynxes in 1998). It is important to determine whether captivity, with no hope of ever returning them the cause or causes that brought the species to to the wild or of recovering the natural extinction in the specific area have been population, would be a pointless exercise. eradicated and, if so, whether there is admin- The breeding programme encourages, coop- istrative and local population support for the erates with and supports media interest in the Program and whether the habitat is prepared Iberian lynx, while taking every opportunity to support a viable population of the species. to remind the public of the primary impor- All re-introductions and translocations must tance of in situ conservation work. be performed using scientific support and We also share on-line information on the the Iberian lynx should be no exception Iberian lynx web page (http://www.lynxexsitu. (Palomares, 2006). Such conservation techni- es), featuring monthly newsletters, pictures and ques require an interdisciplinary approach, videos of all ‘captive’ lynxes, along with with input from experts in ecology, veterinary general interest and scientific articles, and medicine, physiology and behavioural scien- descriptions of the Center’s protocols and ces, as well as support from socio-political working methods. An English-language ver- and information sciences. All stages of pro- sion is currently in production, to further gramme development and implementation expand the scope of communication and must have well-defined protocols that docu- awareness efforts. The Web page also contains ment the objectives, methodology, responsi- an area only accessible to managers, research- bilities, as well as the accountability of the ers and technical personnel working directly organizations and individuals involved. with the Program, for restricted database access The greater the number of captive-bred and other information exchange. As part of its lynxes produced and trained to maximize their training efforts, the Acebuche Center Breeding potential for post-release survival, the lower Program organizes on-site internships for re- the number of wild lynxes that must be cap- cent college graduates interested in acquiring tured to establish new populations, or to re- first-hand knowledge within an endangered inforce the existing ones (Simo´ n & Cadenas, species conservation programme.

2006). Re-introduction and translocation each pose advantages and disadvantages. A com- CONCLUSION parative study is required to determine which option, or combination of options, is most Besides offering an insurance against extinc- appropriate for the conservation of the Iberian tion, the Iberian Lynx Conservation Breeding lynx. Program emphasizes how results from multi- 6. Communication, awareness and training disciplinary life-science research can be Awareness, education and scientiﬁc training integrated into an adaptive management ap- are essential to all conservation-breeding pro- proach to help recover the world’s most grammes. Education and awareness efforts threatened felid species. The ultimate goal of should be focused on changing prevalent the ex situ Program is to offer sound support attitudes that contribute to habitat destruction to in situ conservation efforts by providing and species extinction. One advantage en- healthy Iberian lynx for future re-introduction

projects. In addition, the Program carries out ings: 59–60. Sevilla: Fundacio´ n Biodiversidad; Madrid: a communication plan aimed at preparing Ministerio de Medio Ambiente. http://www.lynxexsitu.es/ documentos/comunicacion/simposios/cursoexsitu06/Iberian professionals for working with threatened- %20Lynx%20Ex-situ%20Conservation.pdf species conservation as well as sensitizing GUZMA´ N, N., GARCIÁ, F., GARROTE, G., PE´ REZ DE AYALA, the general public and decision-makers about R. & IGLESIAS, M. (2002): El lince ibe´rico (Lynx pardinus) the importance of conserving habitat for the en Espan˜ a y Portugal. Censo-diagno´ stico de sus pobla- recovery of this charismatic felid. An effec- ciones. Direccio´ n General para la Biodiversidad, Madrid. HEREDIA, B., GAONA, P., VARGAS, A., SEAL, U. & ELLIS, S. tive recovery of the Iberian lynx in nature will (Eds) (1999): Taller sobre la viabilidad de las pobla- help protect large areas of Mediterranean ciones de lince Ibe´rico (Lynx pardinus). Apple Valley, forests and scrubland, thus benefiting a wide MN: IUCN SSC Conservation Breeding Specialist variety of species that thrive on this unique Group; Madrid: MIMAM. http://lynx.uio.no/lynx/ibe lynxco/20_il-compendium/home/index_es.htm and important ecosystem. IUCN (1998): IUCN guidelines for re-introductions. Gland and Cambridge: IUCN/SSC Re-introduction Spe- ACKNOWLEDGEMENTS cialist Group. http://www.iucn.org/themes/ssc/publica The authors would like to thank all the institutions (and tions/policy/reinte.htm associated staff) that presently collaborate in the Iberian IUCN (2006): 2006 IUCN red list of threatened species. Lynx Conservation Breeding Program, including the Gland and Cambridge: IUCN. http://www.iucnredlist. Spanish Ministry of the Environment, the governments org/ of Andalusia, Extremadura, Castilla-La Mancha and JACOBSON, S. (1991): Evaluation model for developing, Portugal, the Life-Nature Project for Iberian Lynx Con- implementing and assessing conservation education pro- servation in Andalusia, the International Union for the grams: examples from Belize and Costa Rica. Environ- Conservation of Nature (Cat Specialist Group and Con- mental Management 15: 143–150. servation Breeding Specialist Group), the National Scien- JEWGENOW, K., DEHNHARD, M., FRANK, A., NAIDENKO, S., tific Research Council (Don˜ ana Biological Station, the VARGAS, A. & GO¨ RITZ, F. (2006): A comparative analysis National Museum of Natural Sciences, and Almeria Arid of the reproduction of the Eurasian and the Iberian Zones Station), the Seville Diagnostic Analysis Center, lynx in captivity. In Iberian lynx ex-situ conservation the Autonomous University of Barcelona, the Miguel seminar series book of proceedings: 116–117. 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