Biodiversity and Conservation

, Volume 19, Issue 7, pp 2039–2051 | Cite as

Rabbit burrows or artificial refuges are a critical habitat component for the threatened lizard, Timon lepidus (Sauria, Lacertidae)

  • Pierre Grillet
  • Marc Cheylan
  • Jean-Marc Thirion
  • Florian Doré
  • Xavier Bonnet
  • Claude Dauge
  • Sophie Chollet
  • Marc Antoine Marchand
Original Paper


Refuges are crucial for most animal species as they offer essential protection against predators and provide buffered environmental conditions to their occupants. Our data show that northern populations of the threatened ocellated lizard (Timon lepidus) depend on the availability of the burrows excavated by the European rabbit (Oryctolagus cuniculus). In the last decade, a severe decline in rabbit populations has had a disastrous effect on lizard numbers. To compensate for the lack of refuges, artificial shelters were constructed in autumn 2005 and 2007 and were monitored the following years (2006–2009). Most of the artificial refuges were rapidly occupied by lizards, notably juveniles, suggesting that this technique was successful to improve lizard habitat. Because other factors such as food resources might be also crucial, further assessments are required to determine if artificial refuges are sufficient to stem population decline. These results nonetheless provide an encouraging option to maintain and/or to restore threatened populations, for instance through a buffering of rabbit burrow fluctuations. More generally, the availability of suitable refuges (e.g. natural or artificial) is likely to be a central component for the conservation of many reptile species. The combination of empirical and experimental data further demonstrates that great attention must be paid to the structure and distribution of the refuges and that simple practical actions can effectively improve habitat quality for threatened species.


Artificial burrow Timon lepidus Lizard conservation Oryctolagus cuniculus Refuge Reptiles 


  1. Alves PC, Ferrand N, Hackländer K (2008) Lagomorph biology: evolution, ecology, and conservation. Springer, Berlin, Heidelberg, p 414Google Scholar
  2. Anderson PK (1986) Foraging range in mice and voles: the role of risk. Can J Zool 64:2645–2653CrossRefGoogle Scholar
  3. Armstrong JD, Griffiths SW (2001) Density-dependent refuge use among over-wintering wild Atlantic salmon juveniles. J Fish Biol 58:1524–1530CrossRefGoogle Scholar
  4. Beck DD, Jennings RD (2003) Habitat use by Gila monsters: the importance of shelters. Herpetol Monogr 17:111–129CrossRefGoogle Scholar
  5. Berryman AA, Hawkins BA (2006) The refuge as an integrating concept in ecology and evolution. Oikos 115:92–196CrossRefGoogle Scholar
  6. Bonnet X, Brischoux F (2008) Thirsty sea snakes forsake their shelter during rainfall. Austral Ecol 33:911–921CrossRefGoogle Scholar
  7. Bonnet X, Brischoux F, Pearson D, Rivalan P (2009) Beach-rock as a keystone habitat for sea kraits. Environ Conserv 36:62–70CrossRefGoogle Scholar
  8. Bulova SJ (2002) How temperature, humidity, and burrow selection affect evaporative water loss in desert tortoises. J Therm Biol 27:175–189CrossRefGoogle Scholar
  9. Cabral MJ, Almeida J, Almeida PR, Dellinger T, Ferrand de Almeida N, Oliveira ME, Palmeirim JM, Queiroz AI, Rogado L, Santos-Reis M (2005) Livro vermelho dos vertebrados de Portugal (red book of vertebrates of Portugal). Instituto de Conservação da Natureza, Lisboa, p 660Google Scholar
  10. Callou C (1995) Modification de l’aire de répartition du lapin Oryctolagus cuniculus en France et en Espagne du Pléistocène à l’époque actuelle. Etat de la question. Anthropozoologica 21:95–114Google Scholar
  11. Callou C (2003) De la garenne au clapier. Etude archéozoologique du lapin en Europe occidentale. Muséum National d’Histoire Naturelle, Paris, p 358Google Scholar
  12. Castilla AM, Bauwens D, Llorente GA (1991) Diet composition of the lizard Lacerta lepida in Central Spain. J Herpetol 25:30–36CrossRefGoogle Scholar
  13. Cheylan M (1984) Croissance et détermination de l'âge chez le lézard ocellé (groupe Lacerta lepida, Sauria, Lacertidae) de France et du Maroc à partir de la squelettochronologie. Bull Mus Hist Nat Marseille 44:29–37Google Scholar
  14. Cheylan M, Grillet P (2004) Le lézard ocellé. Collection Eveil Nature, Belin, Paris, p 95Google Scholar
  15. Cheylan M, Grillet P (2005) Statut passé et actuel du lézard ocellé (Lacerta lepida, Sauriens, Lacertidés) en France. Implication en terme de conservation. Vie Milieu 55:15–30Google Scholar
  16. Clobert J, Danchin E, Dhondt AA, Nichols JD (2001) Dispersal. Oxford University Press, OxfordGoogle Scholar
  17. Clobert J, Le Galliard J-F, Cote J, Massot M, Meylan S (2009) Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ideas and Perspectives. Ecol Lett 12:197–209CrossRefPubMedGoogle Scholar
  18. Cooper CE, Withers PC (2005) Physiological significance of the microclimate in night refuges of the numbat Myrmecobius fasciatus. Aust Mammal 27:169–174Google Scholar
  19. Cosepac (2004) Evaluation et Rapport de situation du COSEPAC sur les couleuvres agiles à ventre jaune de l’Est et de l’Ouest (Coluber constrictor flaviventris et Coluber constrictor mormon) au Canada. Mise à jour. Comité sur la situation des espèces en péril au Canada. Ottawa. VII + 39 p.
  20. Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R (2008) Key role of European rabbits in the conservation of the western Mediterranean basin hotspot. Conserv Biol 22:1106–1117CrossRefPubMedGoogle Scholar
  21. Diaz JA, Monasterio C, Salvador A (2006) Abundance, microhabitat selection and conservation of eyed lizards (Lacerta lepida): a radiotelemetric study. J Zool 268:295–301CrossRefGoogle Scholar
  22. Doré F (2008) Mise en place d’un suivi à long terme et caractérisation des habitats d’une population de Lézard ocellé Timon lepidus (Daudin, 1802) en limite nord de répartition sur l’île d’Oléron. Mémoire de Master 2. Ecole Pratique des Hautes Etudes, Montpellier, p 37Google Scholar
  23. Gálvez Bravo L, Belliure J, Rebollo S (2009) European rabbits as ecosystem engineers: warrens increase lizard density and diversity. Biodivers Conserv 18:869–885CrossRefGoogle Scholar
  24. Goldsbrough CL, Hochuli DF, Shine R (2004) Thermal cues used for retreat-site selection by flat rock spiders confer fitness benefits. Ecology 85:1635–1641CrossRefGoogle Scholar
  25. Grillet P, Cheylan M, Dusoulier F (2006) Evolution des habitats et changement climatique : quelles conséquences pour les populations de lézard ocellé, Lacerta lepida (Saurien, Lacertidés), en limite nord de répartition? Ecol Mediterr 32:63–72Google Scholar
  26. Grillet P, Doré F, Thirion JM, Cheylan M, Dauge C (2008) Etude et suivi de la population de Lézard ocellé Timon lepidus sur l’île d’Oléron. Rapport d’étude 2008. Office National des Forêts, Poitiers, p 94Google Scholar
  27. Hódar JA, Campos F, Rosales BA (1996) Trophic ecology of the Ocellated Lizard Lacerta lepida in an arid zone of southern Spain: relationships with availability and daily activity of prey. J Arid Environ 33:95–107CrossRefGoogle Scholar
  28. Kessler J, Chambraud A (1990) La météo de la France. Tous les climats localité par localité. J.-C. Lattès, ParisGoogle Scholar
  29. Kotler BP, Brown SJ, Bouskila A (2004) Apprehension and time allocation in gerbils: the effects of predatory risk and energetic state. Ecology 85:917–922CrossRefGoogle Scholar
  30. Lahondère C (1980) Les dunes du Centre-Ouest : le milieu physique. In La vie dans les dunes du Centre-Ouest, flore et faune. Bull Soc Bot Centre-Ouest (Numéro Spécial) 4:18–24Google Scholar
  31. Letty J, Queney G, Gautier A, Marchandeau S (2005) Evaluation de l’efficacité des repeuplements par suivi génétique: l’exemple du lapin de garenne. Faune Sauvage 265:39–46Google Scholar
  32. Lopez-Martinez N (2008) The Lagomorph Fossil record and the origin of the European Rabbit. In: Alves PC, Ferrand N, Hackländer K (eds) Lagomorph biology: evolution, ecology, and conservation. Springer, Berlin, Heidelberg, pp 27–46Google Scholar
  33. Mateo JA (2008) Lagarto ocelado—Timon lepidus. In: Carrascal LM, Salvador A (eds) Enciclopedia virtual de los vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid.
  34. Millidine KJ, Armstrong JD, Metcalfe NB (2006) Presence of shelter reduces maintenance metabolism of juvenile salmon. Funct Ecol 20:839–845CrossRefGoogle Scholar
  35. Paulo OF (1988) Estudo eco-etologico da populaçao de Lacerta lepida (Daudin, 1802) da ilha de Berlenga. Relatorio de estagio de licencatura en biologia. FCUL, Lisboa, p 314Google Scholar
  36. Paulo OS, Pinheiro J, Miraldo A, Bruford MW, Jordan WC, Nichols RA (2008) The role of vicariance vs. dispersal in shaping genetic patterns in ocellated lizard species in the western Mediterranean. Mol Ecol 17:1535–1551CrossRefGoogle Scholar
  37. Pleguezuelos JM, Márquez R, Lizana M (eds) (2002) Atlas y libro rojo de los Anfibios y los reptiles de España. Dirección General de Conservación de la Naturaleza—Asociación Herpetologica Española, Madrid, p 587Google Scholar
  38. Read JL, Carter J, Moseby KM, Greenville A (2008) Ecological roles of rabbit, bettong and bilby warrens in arid Australia. J Arid Environ 72:2124–2130CrossRefGoogle Scholar
  39. Real J (1996) Biases in diet study methods in the Bonelli’s eagle. J Wildlife Manag 60:632–638CrossRefGoogle Scholar
  40. Reichmann OJ, Smith ST (1990) Burrows and burrowing behaviour by mammals. In: Genoways HH (ed) Current mammalogy. Plenum Press, New York, pp 197–244Google Scholar
  41. Roper TJ, Bennet NC, Conrad TL, Molteno AJ (2001) Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. J Zool (Lond) 254:101–107CrossRefGoogle Scholar
  42. Schwarzkopf L, Alford RA (1996) Desiccation and shelter-site use in a tropical amphibian: comparing toads with physical models. Funct Ecol 10:193–200CrossRefGoogle Scholar
  43. Shine R, Bonnet X (2009) Reproductive biology, population viability and options for field management. In: Mullin SJ, Seigel RA (eds) Snakes: ecology and conservation. Cornell University Press, Ithaca, New YorkGoogle Scholar
  44. Sih A (1997) To hide or not to hide? Refuge use in a fluctuating environment. TREE 12:375–376Google Scholar
  45. Souter NJ, Bull CM, Hutchinson MN (2004) Adding burrows to enhance a population of the endangered pygmy blue tongue lizard Tiliqua adelaidensis. Biol Conserv 116:403–408CrossRefGoogle Scholar
  46. Thirion JM, Grillet P (2002) Le lapin de garenne : une espèce clé dans nos écosystèmes. Société Nationale de Protection de la Nature. Cour Nat 202:21–23Google Scholar
  47. Thirion JM, Grillet P, Geniez Ph (2002) Les Amphibiens et les Reptiles du centre-ouest de la France. Région Poitou-Charentes et départements limitrophes. Collection Parthénope, Éditions Biotope, Mèze, p 144Google Scholar
  48. Thirion JM, Grillet P, Cheylan M (2009) Composition et variation saisonnière du régime alimentaire du lézard ocellé Timon lepidus sur l’île d’Oléron (France) à partir des fèces. Revue d’ Ecologie (la Terre et la Vie) 64:239–250Google Scholar
  49. Vicente LA (1989). Sobre a historia natural dos repteis da ilha Berlenga, sindrome de insularidade. Dissertaçao de Doutoramento, Faculdad de Ciencias, Uuniversidade de Lisboa, 485 ppGoogle Scholar
  50. Villafuerte R, Calvete C, Blanco JC, Lucientes J (1995) Incidence of viral hemorrhagic disease in wild rabbit populations in Spain. Mammalia 59:651–659CrossRefGoogle Scholar
  51. Ward D (2005). Reversing Rabbit Decline: one of the biggest challenges for nature conservation in Spain and Portugal. Field Reports. UICN/SSC, Lagomorph Specialist Group, 54 ppGoogle Scholar
  52. Webb JK, Shine R (2000) Paving the way for habitat restoration: can artificial rocks restore degraded habitats for endangered reptiles? Biol Conserv 92:93–99CrossRefGoogle Scholar
  53. Williams JB, Tieleman BI, Shobrak M (1999) Lizard burrows provide thermal refugia for larks in the Arabian Desert. Condor 101:714–717CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Pierre Grillet
    • 1
  • Marc Cheylan
    • 1
  • Jean-Marc Thirion
    • 2
  • Florian Doré
    • 2
  • Xavier Bonnet
    • 3
  • Claude Dauge
    • 4
  • Sophie Chollet
    • 2
  • Marc Antoine Marchand
    • 2
  1. 1.Ecologie et Biogéographie des Vertébrés, EPHE-CEFE-CNRSMontpellierFrance
  2. 2.OBIOSPont l’Abbé d’ArnoultFrance
  3. 3.CEBC-CNRSVilliers en BoisFrance
  4. 4.Office National des Forêts, MaisonSaint TrojanFrance

Personalised recommendations