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

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Abstract

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.

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References

  • Adolph SC (1990) Influence of behavioural thermoregulation on microhabitat use by two Sceloporus lizards. Ecology 71:315–327

    Article  Google Scholar 

  • 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 82:897–901

    Article  Google Scholar 

  • Bangert RK, Slobodchikoff CN (2006) Conservation of prairie dog ecosystem engineering may support artjropod beta and gamma diversity. J Arid Environ 67:100–115

    Article  Google Scholar 

  • Bauwens D, Garland T Jr, Castilla AM, Van Damme R (1995) Evolution of sprint speed in lacertid lizards: morphological, physiological and behavioral covariation. Evolution 49:848–863

    Article  Google Scholar 

  • Bennet NC (1980) The thermal dependence of lizard behaviour. Anim Behav 28:752–762

    Article  Google Scholar 

  • Blanco JC (1998) Mamíferos de España II. Editorial Planeta, Barcelona

    Google Scholar 

  • 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 222:692–693

    Google Scholar 

  • Calvete C, Villafuerte R, Lucientes J, Osácar JJ (1997) Effectiveness of traditional wild rabbit restocking in Spain. J Zool 241:271–277

    Article  Google Scholar 

  • Calzolai R, Chelazzi G (1991) Habitat use in a central Italy population of Testudo hermanni Gmelin (Reptilia testudinae). Ethol Ecol Evol 3:153–166

    Google Scholar 

  • 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 259–261

    Google Scholar 

  • 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 262–264

    Google Scholar 

  • Castilla AM, Swallow JG (1995) Artificial egg-laying sites for lizards: a conservation strategy. Biol Conserv 72:387–391

    Article  Google Scholar 

  • 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 York

    Google Scholar 

  • 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 150:282–290

    Article  Google Scholar 

  • Delibes-Mateos M, Redpath SM, Angulo E, Ferreras P, Villafuerte R (2007) Rabbits as keystone species in southern Europe. Biol Conserv 137:149–156

    Article  Google Scholar 

  • Díaz JA, Carrascal LM (1991) Regional distribution of a mediterranean lizard: influence of habitat cues and prey abundance. J Biogeogr 18:291–297

    Article  Google Scholar 

  • 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 3:235–240

    Google Scholar 

  • Downes S, Shine R (1998) Heat, safety or solitude? Using habitat selection experiments to identify a lizard’s priorities. Anim Behav 55:1387–1396

    Article  PubMed  Google Scholar 

  • 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 125–140

    Google Scholar 

  • 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 32:723–731

    Article  Google Scholar 

  • Hawkins LK, Nicoletto PF (1992) Kangaroo rat burrows structure the spatial organization of ground-dwelling animals in a semiarid grassland. J Arid Environ 23:199–208

    Google Scholar 

  • 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 244–246

  • 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 70:931–944

    Article  Google Scholar 

  • Iraeta P, Monasterio C, Salvador A, Díaz JA (2006) Mediterranean hatchling lizards grow faster at higher altitude: a reciprocal transplant experiment. Funct Ecol 20:865–872

    Article  Google Scholar 

  • Jefferies RL (2000) Allochthonous inputs: integrating population changes and food web dynamics. Trends Ecol Evol 15:19–22

    Article  PubMed  Google Scholar 

  • 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 124:205–213

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  • Kay FR, Whitford WG (1978) The burrow environment of the banner-tailed kangaroo rat, Dipodomys spectabilis, in South-central New Mexico. Am Midl Nat 99:270–279

    Article  Google Scholar 

  • Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145

    Article  Google Scholar 

  • Kretzer JE, Cully JF (2001) Effects of black-tailed prairie dogs on reptiles and amphibians in Kansas shortgrass prairie. Southwest Nat 46:171–177

    Article  Google Scholar 

  • Kruess A, Tscharntke T (2002) Contrasting responses of plant and insect diversity to variation in grazing intensity. Biol Conserv 106:293–302

    Article  Google Scholar 

  • Lai CH, Smith AT (2003) Keystone status of plateau pikas (Ochotona curzoniae): effect of control on biodiversity of native birds. Biodivers Conserv 12:1901–1912

    Article  Google Scholar 

  • Lomolino MV, Smith GA (2003) Terrestrial vertebrate communities at black-tailed prairie dog (Cynomys ludovicianus) towns. Biol Conserv 115:89–100

    Article  Google Scholar 

  • 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 9:293–299

    Google Scholar 

  • Martín J, López P (2002) The effect of Mediterranean dehesa management on lizard distribution and conservation. Biol Conserv 108:213–219

    Article  Google Scholar 

  • Martín J, Salvador A (1995) Microhabitat selection by the Iberian rock lizard Lacerta monticola: effects on density and spatial distribution of individuals. Biol Conserv 79:303–307

    Article  Google Scholar 

  • McBrayer LD, Reilly SM (2002) Prey processing in lizards: behavioral variation in sit-and-wait and widely foraging taxa. Can J Zool 80:882–892

    Article  Google Scholar 

  • Ministerio de Agricultura PYA (1989) Caracterización agroclimática de la provincia de Madrid. Madrid, p 120

  • 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 73:81–85

    Article  Google Scholar 

  • Moreno S, Villafuerte R, Cabezas S, Lombardi L (2004) Wild rabbit restocking for predator conservation in Spain. Biol Conserv 118:183–193

    Article  Google Scholar 

  • 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 337–361

  • Pérez-Mellado V (1998) Acanthodactylus erythrurs (Schinz, 1834) In: Salvador A (Coord.) Reptiles. Fauna Ibérica, vol 10. Museo Nacional de Ciencias Naturales, Madrid, pp 167–175

  • Perry G, Garland TJ (2002) Lizard home ranges revisited: effects of sex, body size, diet, habitat and phylogeny. Ecology 83:1870–1885

    Article  Google Scholar 

  • Pianka ER (1966) Convexity, desert lizards, and spatial heterogeneity. Ecology 47:1055–1059

    Article  Google Scholar 

  • Pielou EC (1966) The measurement of diversity in different types of biological collections. J Theor Biol 13:131–144

    Article  Google Scholar 

  • Pollo CJ, Pérez-Mellado V (1991) An analysis of a Mediterranean assemblage of three small lacertid lizards in Central Spain. Acta Oecol 12:655–671

    Google Scholar 

  • Reichman OJ, Seabloom EW (2002) The role of pocket gophers as subterranean ecosystem engineers. Trends Ecol Evol 17:44–50

    Article  Google Scholar 

  • 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 255:291–299

    Article  Google Scholar 

  • 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 16:691–703

    Article  Google Scholar 

  • Salvador A (1982) A revisión of the lizards of the genus Acanthodactylus (Sauria: Lacertidae). Bonn Zool Monogr 16:1–167

    Google Scholar 

  • 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 66:27–41

    Article  Google Scholar 

  • 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 244–246

  • van Heerden J, Dauth J (1987) Aspects of adaptation to an arid environments in free-living ground squirrels Xerus inauris. J Arid Environ 13:83–89

    Google Scholar 

  • 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 52:345–356

    Google Scholar 

  • 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 16:3489–3504

    Article  Google Scholar 

  • Whicker AD, Detling JK (1998) Ecological consequences of prairie dog disturbances. Bioscience 38:778–785

    Article  Google Scholar 

  • Whitford WG, Kay FR (1999) Biopedturbation by mammals in deserts: a review. J Arid Environ 41:203–230

    Article  Google Scholar 

  • Wiens JA (1984) Resource systems, populations and communities. In: Price PW, Slobodchikoff CM, Gaud WS (eds) A new ecology. Wiley, New York, pp 397–436

    Google Scholar 

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Acknowledgements

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.

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Gálvez Bravo, L., Belliure, J. & Rebollo, S. European rabbits as ecosystem engineers: warrens increase lizard density and diversity. Biodivers Conserv 18, 869–885 (2009). https://doi.org/10.1007/s10531-008-9438-9

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  • DOI: https://doi.org/10.1007/s10531-008-9438-9

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