Biodiversity and Conservation

, Volume 18, Issue 4, pp 869–885 | Cite as

European rabbits as ecosystem engineers: warrens increase lizard density and diversity

  • Lucía Gálvez Bravo
  • Josabel Belliure
  • Salvador Rebollo
Original Paper


Mammals that build extensive open burrow systems are often classified as ecosystem engineers, since they have the potential to modulate the availability of resources for themselves and other organisms. Lizards may benefit from the heterogeneity created by these structures, especially if coupled with an increased offer of sites for refuge and thermoregulation. However, information about these engineering effects by burrowing animals is scarce. We investigated the influence of European rabbit burrows on several parameters of a Mediterranean lizard community (abundance, density, diversity and body condition) in three different habitats (open pastures, holm oak and scrub patches). We found that lizards were positively associated with burrows, and that burrows determined lizard presence at otherwise unfavourable habitats. Moreover, community parameters such as density and species richness were higher in sites with burrows. Burrows influenced lizard species in different ways, and were also relevant for other Mediterranean vertebrates, as revealed by questionnaires to experts. We also explored the possible resources provided by burrows for lizards. Warrens offer relatively abundant prey and appropriate retreat sites for refuge and thermoregulation. Warrens may have further implications within the ecosystem, acting as stepping stones, allowing lizards to reach otherwise inaccessible habitat patches. This study shows that European rabbit warrens have a positive influence on lizard density and diversity, and confirms the role of rabbits as ecosystem engineers. This reinforces the need for appropriate conservation measures for rabbits, especially given their threatened status in the Iberian Peninsula. Furthermore, our study highlights that taking into account the influence of engineering activities increases our awareness of species interactions, and may translate into more adequate conservation measures for the preservation of biodiversity.


Burrows Dehesa Mediterranean Oryctolagus cuniculus Stepping stones 



We are very grateful to Gonzalo García, Alberto González, Carlota Martínez and Itziar Rodríguez for their help with fieldwork. Thanks to all the experts that replied to our questionnaires; and thanks to Luis Cayuela and two anonymous reviewers for valuable comments on a previous version of this manuscript. This study was funded by projects REN2000-0783/GLO and REN 2003-05553/GLO, Ministerio de Ciencia y Tecnología. Lucía Gálvez Bravo was supported by a FPI grant from the Comunidad de Madrid throughout the duration of this study.


  1. Adolph SC (1990) Influence of behavioural thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71:315–327CrossRefGoogle Scholar
  2. Amo L, López P, Martín J (2004) Trade-offs in the choice of refuges by common wall lizards: do thermal costs affect preferences for predator-free refuges? Can J Zool 82:897–901CrossRefGoogle Scholar
  3. Bangert RK, Slobodchikoff CN (2006) Conservation of prairie dog ecosystem engineering may support artjropod beta and gamma diversity. J Arid Environ 67:100–115CrossRefGoogle Scholar
  4. Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioral covariation. Evolution 49:848–863CrossRefGoogle Scholar
  5. Bennet NC (1980) The thermal dependence of lizard behaviour. Anim Behav 28:752–762CrossRefGoogle Scholar
  6. Blanco JC (1998) Mamíferos de España II. Editorial Planeta, BarcelonaGoogle Scholar
  7. Blazquez MC, Villafuerte R (1990) Nesting of the Montpellier snake (Malpolon monspessulanus) inside rabbit warrens ate Doñana National Park (SW Spain): phenology and a probable case of communal nesting. J Zool 222:692–693Google Scholar
  8. Calvete C, Villafuerte R, Lucientes J, Osácar JJ (1997) Effectiveness of traditional wild rabbit restocking in Spain. J Zool 241:271–277CrossRefGoogle Scholar
  9. Calzolai R, Chelazzi G (1991) Habitat use in a central Italy population of Testudo hermanni Gmelin (Reptilia testudinae). Ethol Ecol Evol 3:153–166Google Scholar
  10. Carretero MA, Montori A, Llorente GA, Santos X (2002a) Psammodromus algirus. In: Pleguezuelos JM, Márquez R, Liziana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza, Madrid, pp 259–261Google Scholar
  11. Carretero MA, Santos T, Montori A, Llorente GA (2002b) Psammodromus hispanicus. In: Pleguezuelos JM, Márquez R, Liziana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza, Madrid, pp 262–264Google Scholar
  12. Castilla AM, Swallow JG (1995) Artificial egg-laying sites for lizards: a conservation strategy. Biol Conserv 72:387–391CrossRefGoogle Scholar
  13. Christensen NL (1997) Managing for heterogeneity and complexity on dynamic landscapes. In: Pickett STA, Ostfeld RS, Shachak M, Likens GE (eds) The ecological basis for conservation: heterogeneity, ecosystems, and biodiversity. Chapman and Hall, New YorkGoogle Scholar
  14. Davis JR, Theimer TC (2003) Increased lesser earless lizard (Holbrookia maculata) abundance on gunnison’s prairie dog colonies and short term responses to artificial prairie dog burrows. Am Midl Nat 150:282–290CrossRefGoogle Scholar
  15. Delibes-Mateos M, Redpath SM, Angulo E, Ferreras P, Villafuerte R (2007) Rabbits as keystone species in southern Europe. Biol Conserv 137:149–156CrossRefGoogle Scholar
  16. Díaz JA, Carrascal LM (1991) Regional distribution of a mediterranean lizard: influence of habitat cues and prey abundance. J Biogeogr 18:291–297CrossRefGoogle Scholar
  17. Díaz JA, Carbonell R, Virgós E, Santos T, Tellería JL (2000) Effects of forest fragmentation on the distribution of the lizard Psammodromus algirus. Anim Conserv 3:235–240Google Scholar
  18. Downes S, Shine R (1998) Heat, safety or solitude? Using habitat selection experiments to identify a lizard’s priorities. Anim Behav 55:1387–1396PubMedCrossRefGoogle Scholar
  19. Gálvez L, López-Pintor A, De Miguel JM, Alonso G, Rueda M, Rebollo S, Gómez-Sal A (2008) Ecosystem engineering effects of European rabbits in a Mediterranean habitat. In: Alves PC, Ferrand N, Hackländer K (eds) Lagomorph biology, evolution, ecology and conservation. Springer-Verlag, Berlin, pp 125–140Google Scholar
  20. Gea-Izquierdo G, Muñoz-Igualada J, San Miguel-Ayanz A (2005) Rabbit warren distribution in relation to pasture communities in Mediterranean habitats: consequences for management of rabbit populations. Wildlife Res 32:723–731CrossRefGoogle Scholar
  21. Hawkins LK, Nicoletto PF (1992) Kangaroo rat burrows structure the spatial organization of ground-dwelling animals in a semiarid grassland. J Arid Environ 23:199–208Google Scholar
  22. Hódar JA (2002) Acanthodactylus erythrurus. In: Pleguezuelos JM, Márquez R, Liziana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España, Madrid, pp 244–246Google Scholar
  23. Huey RB, Peterson CR, Arnold SJ, Porter WP (1989) Hot rocks and not-so-hot rocks: retreat-site selection by garter snakes and its thermal consequences. Ecology 70:931–944CrossRefGoogle Scholar
  24. Iraeta P, Monasterio C, Salvador A, Díaz JA (2006) Mediterranean hatchling lizards grow faster at higher altitude: a reciprocal transplant experiment. Funct Ecol 20:865–872CrossRefGoogle Scholar
  25. Jefferies RL (2000) Allochthonous inputs: integrating population changes and food web dynamics. Trends Ecol Evol 15:19–22PubMedCrossRefGoogle Scholar
  26. Ji X, Braña F (1999) The influence of thermal and hydric environments on embryonic use of energy and nutrients, and hatchling traits, in the wall lizards (Podarcis muralis). Comp Biochem Phys A 124:205–213CrossRefGoogle Scholar
  27. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  28. Kay FR, Whitford WG (1978) The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in South-central New Mexico. Am Midl Nat 99:270–279CrossRefGoogle Scholar
  29. Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145CrossRefGoogle Scholar
  30. Kretzer JE, Cully JF (2001) Effects of black-tailed prairie dogs on reptiles and amphibians in Kansas shortgrass prairie. Southwest Nat 46:171–177CrossRefGoogle Scholar
  31. Kruess A, Tscharntke T (2002) Contrasting responses of plant and insect diversity to variation in grazing intensity. Biol Conserv 106:293–302CrossRefGoogle Scholar
  32. Lai CH, Smith AT (2003) Keystone status of plateau pikas (Ochotona curzoniae): effect of control on biodiversity of native birds. Biodivers Conserv 12:1901–1912CrossRefGoogle Scholar
  33. Lomolino MV, Smith GA (2003) Terrestrial vertebrate communities at black-tailed prairie dog (Cynomys ludovicianus) towns. Biol Conserv 115:89–100CrossRefGoogle Scholar
  34. Markwell TJ, Daugherty CH (2002) Invertebrate and lizard abundance is greater on seabird-inhabited islands than on seabird-free islands in the Marlborough Sounds, New Zealand. Ecoscience 9:293–299Google Scholar
  35. Martín J, López P (2002) The effect of Mediterranean dehesa management on lizard distribution and conservation. Biol Conserv 108:213–219CrossRefGoogle Scholar
  36. Martín J, Salvador A (1995) Microhabitat selection by the Iberian rock lizard Lacerta monticola: effects on density and spatial distribution of individuals. Biol Conserv 79:303–307CrossRefGoogle Scholar
  37. McBrayer LD, Reilly SM (2002) Prey processing in lizards: behavioral variation in sit-and-wait and widely foraging taxa. Can J Zool 80:882–892CrossRefGoogle Scholar
  38. Ministerio de Agricultura PYA (1989) Caracterización agroclimática de la provincia de Madrid. Madrid, p 120Google Scholar
  39. Moreno S, Villafuerte R (1995) Traditional management of scrubland for the conservation of rabbits Oryctolagus cuniculus and their predators in Doñana National Park, Spain. Biol Conserv 73:81–85CrossRefGoogle Scholar
  40. Moreno S, Villafuerte R, Cabezas S, Lombardi L (2004) Wild rabbit restocking for predator conservation in Spain. Biol Conserv 118:183–193CrossRefGoogle Scholar
  41. Pérez-Mellado V (1992) Los anfibios y reptiles de la dehesa. In: El libro de las dehasas salmantinas Gómez Gutiérrez JMC (ed) Junta de Castilla y León, Consejería de Medio Ambiente y O.T., Salamanca. pp 337–361Google Scholar
  42. Pérez-Mellado V (1998) Acanthodactylus erythrurs (Schinz, 1834) In: Salvador A (Coord.) Reptiles. Fauna Ibérica, vol 10. Museo Nacional de Ciencias Naturales, Madrid, pp 167–175Google Scholar
  43. Perry G, Garland TJ (2002) Lizard home ranges revisited: effects of sex, body size, diet, habitat and phylogeny. Ecology 83:1870–1885CrossRefGoogle Scholar
  44. Pianka ER (1966) Convexity, desert lizards, and spatial heterogeneity. Ecology 47:1055–1059CrossRefGoogle Scholar
  45. Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144CrossRefGoogle Scholar
  46. Pollo CJ, Pérez-Mellado V (1991) An analysis of a Mediterranean assemblage of three small lacertid lizards in Central Spain. Acta Oecol 12:655–671Google Scholar
  47. Reichman OJ, Seabloom EW (2002) The role of pocket gophers as subterranean ecosystem engineers. Trends Ecol Evol 17:44–50CrossRefGoogle Scholar
  48. Revilla E, Palomares F, Fernández N (2001) Characteristics, location and selection of diurnal resting dens by Eurasian badgers (Meles meles) in a low density area. J Zool 255:291–299CrossRefGoogle Scholar
  49. Rogers PM, Myers K (1979) Ecology of the European wild rabbit Oryctolagus cuniculus (L.) in Mediterranean habitats. I. Distribution in the landscape of the coto Doñana, Spain. J Appl Ecol 16:691–703CrossRefGoogle Scholar
  50. Salvador A (1982) A revisión of the lizards of the genus Acanthodactylus (Sauria: Lacertidae). Bonn Zool Monogr 16:1–167Google Scholar
  51. Shipley BK, Reading RP (2006) A comparison of the herpetofauna and small mammal diversity on black-tailed prairie dog (Cynomys ludovicianus) colonies and non-colonized grasslands in Colorado. J Arid Environ 66:27–41CrossRefGoogle Scholar
  52. Sousa P, Pérez-Mellado V (2002) Podarcis hispanica. In: Pleguezuelos JM, Márquez R, Liziana M (eds) Atlas y Libro Rojo de los Anfibios y Reptiles de España, Madrid, pp 244–246Google Scholar
  53. van Heerden J, Dauth J (1987) Aspects of adaptation to an arid environments in free-living ground squirrels Xerus inauris. J Arid Environ 13:83–89Google Scholar
  54. Villafuerte R, Lazo A, Moreno S (1997) Influence of food abundance and quality on rabbit fluctuations: conservation and management implications in Doñana National park (SW Spain). Rev Écol-Terre Vie 52:345–356Google Scholar
  55. Virgós E, Cabezas-Díaz S, Lozano J (2007) Is the wild rabbit (Oryctolagus cuniculus) a threatened species in spain? Sociological constraints in the conservation of species. Biodivers Conserv 16:3489–3504CrossRefGoogle Scholar
  56. Whicker AD, Detling JK (1998) Ecological consequences of prairie dog disturbances. Bioscience 38:778–785CrossRefGoogle Scholar
  57. Whitford WG, Kay FR (1999) Biopedturbation by mammals in deserts: a review. J Arid Environ 41:203–230CrossRefGoogle Scholar
  58. Wiens JA (1984) Resource systems, populations and communities. In: Price PW, Slobodchikoff CM, Gaud WS (eds) A new ecology. Wiley, New York, pp 397–436Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Lucía Gálvez Bravo
    • 1
  • Josabel Belliure
    • 1
  • Salvador Rebollo
    • 1
  1. 1.Departamento de EcologíaUniversidad de Alcalá. Edif. de CienciasAlcala de Henares, MadridSpain

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