The fall of a symbol? A high predation rate by the introduced horseshoe whip snake Hemorrhois hippocrepis paints a bleak future for the endemic Ibiza wall lizard Podarcis pityusensis

  • Arlo Hinckley
  • Elba Montes
  • Enrique Ayllón
  • Juan M PleguezuelosEmail author
Original Article


Invasive species currently account for a major threat to global biodiversity, and island ecosystems are among the most vulnerable, because of the frequency and success of species introductions on islands. Within Mediterranean islands, reptiles not only are frequently introduced species but are also among the most threatened because of these introductions. The Balearic archipelago is a good example of this, since only two of its current 16 species of reptiles are native. Thirteen years ago, the snake Hemorrhois hippocrepis was introduced by cargo in Ibiza island, and it is in expansion. Individuals obtained from an early eradication campaign showed a fast expression of phenotypic plasticity and acquired larger sizes than those of the source population, probably due to a high prey availability and predator scarcity. The species is thriving at the expense of a small variety of native and non-native prey, but the predation pressure on the endemic Podarcis pityusensis, the only native reptile in the island, is very high, as this lizard represents 56% of the prey in frequency, which might threaten its survival on the long term. Our results on the feeding ecology of the snake are of sufficient concern to justify the maintenance of actions to eradicate this invader.


Balearic islands Hemorrhois hippocrepis Invasive species Snake Lizard 



Many people helped in the field and laboratory, like M. Feriche, E. Alaminos, J. Azor, T. Alcover, and the people of the COFIB. X. Santos improved a first draft of this manuscript. Samples have been collected according to the permits issued by the Balearic Government (ESP 26/2014). This work was supported by the Ibiza Insular Council, Balearic Government (grant numbers 54/2013 and 21/2015—AGRICULTURA).


  1. Alcover JA, Moyà-Solà S, Moyà JP (1981) Les quimeres del passat: Els vertebrats fòssils del Plio-Quaternari de les Balears i Pitiüses. Moll, Palma de MallorcaGoogle Scholar
  2. Alivizatos H, Goutner V, Zogaris S (2005) Contribution to the study of the diet of four owl species (Aves, Strigiformes) from mainland and island areas of Greece. Belg J Zool 135:109–118Google Scholar
  3. Almeida D, Almodóvar A, Nicola GG, Elvira B, Grossman GD (2012) Trophic plasticity of invasive juvenile largemouth bass Micropterus salmoides in Iberian streams. Fish Res 113:153–158. doi: 10.1016/j.fishres.2011.11.002 CrossRefGoogle Scholar
  4. Arnold SJ (1993) Foraging theory and prey size-predator size relations in snakes. In: Seigel RA, Collins JT (eds) Snakes: ecology and behavior. McGraw-Hill, New York, pp. 87–115Google Scholar
  5. Aubret F (2015) Island colonization and the evolutionary rates of body size in insular neonate snakes. Heredity 115:349–356. doi: 10.1038/hdy.2014.65 CrossRefPubMedGoogle Scholar
  6. Aubret F, Maumelat S, Bradshaw D, Schwaner T, Bonnet X (2004) Diet divergence, jaw size and scale counts in two neighbouring populations of tiger snakes (Notechis scutatus). Amph-Rep 25:9–17 doi: 10.1163/156853804322992797
  7. Ayllón E (2015) La culebra de herradura (Hemorrhois hippocrepis) en las islas Baleares. Bol Asoc Herpetol Esp 26:88–91Google Scholar
  8. Boback SM (2003) Body size evolution in snakes: evidence from island populations. Copeia 2003:81–94. doi: 10.1643/0045-8511(2003)003[0081: BSEISE]2.0.CO;2 CrossRefGoogle Scholar
  9. Bonnet X, Naulleau G, Lourdais O (2003) The benefits of complementary techniques: using capture-recapture and physiological approaches to understand costs of reproduction in the asp viper. In: Schuett GW, Hoggren M, Douglas ME, Greene HW (eds) Biology of the vipers. Eagle Mountain Publ, Utah, pp. 483–495Google Scholar
  10. Bonnet X, Naulleau G, Shine R, Lourdais O (2001) Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis. Oikos 92:297–308. doi: 10.1034/j.1600-0706.2001.920212.x CrossRefGoogle Scholar
  11. Bover P, Quintana J, Alcover JA (2008) Three islands, three worlds: paleogeography and evolution of the vertebrate fauna from the Balearic islands. Quat Int 182:135–144. doi: 10.1016/j.quaint.2007.06.039 CrossRefGoogle Scholar
  12. Brooks TM, Mittermeier RA, da Fonseca GA, Gerlach J, Hoffmann M, Lamoreux JF, Rodrigues AS (2006) Global biodiversity conservation priorities. Science 313(5783):58–61. doi: 10.1126/science.1127609 CrossRefPubMedGoogle Scholar
  13. Capula M (1994) Population genetics of a colonizing lizard: loss of variability in introduced populations of Podarcis sicula. Experientia 50:691–696CrossRefGoogle Scholar
  14. Carretero MA (2004) From set menu to a la carte. Linking issues in trophic ecology of Mediterranean lacertids. Ital J Zool 71:121–133. doi: 10.1080/11250000409356621 CrossRefGoogle Scholar
  15. Cattaneo A (2015) Contributo alla conoscenza dei serpenti delle isole del canale di Sicilia. Naturalista Siciliano S IV 34:3–28Google Scholar
  16. Cheylan M, Guillaume CP (1993) Elaphe scalaris (Schinz, 1822)—Treppennatter. In: Böhme W (ed) Handbuch der Reptilien und Amphibien Europas. Band 3/I: Schlangen (Serpentes). Aula-Verlag, Wiesbaden, pp. 397–429Google Scholar
  17. Clevenger AP (1993) Pine marten (Martes martes Linné, 1758) comparative feeding ecology in an island and mainland population of Spain. Z Saugetierkd 58:212–212Google Scholar
  18. Close DA, Fitzpatrick MS, Li HW (2002) The ecological and cultural importance of a species at risk of extinction, Pacific lamprey. Fisheries 27:19–25CrossRefGoogle Scholar
  19. Corti C, Luiselli L, Filippi E, Capula M (2000) Distribution, natural history and morphometrics of the critically endangered Coluber hippocrepis populations of Sardinia: a review, with additional data and conservation implications. Amphib-Reptil 21:279–287. doi: 10.1163/156853800507471 CrossRefGoogle Scholar
  20. Garibaldi A, Turner N (2004) Cultural keystone species: implications for ecological conservation and restoration. Ecol Soc 9(3):1. doi: 10.2993/0278-0771-35.3.427 CrossRefGoogle Scholar
  21. Gosàlbez J (1987) Insectívors i rosegadors de Catalunya. Ketres, BarcelonaGoogle Scholar
  22. Greenlees MJ, Brown GP, Webb JK, Phillips BL, Shine R (2006) Effects of an invasive anuran [the cane toad (Bufo marinus)] on the invertebrate fauna of a tropical Australian floodplain. Anim Conserv 9:431–438. doi: 10.1111/j.1469-1795.2006.00057.x CrossRefGoogle Scholar
  23. Guicking D, Griffiths RA, Moore RD, Joger U, Wink M (2006) Introduced alien or persecuted native? Resolving the origin of the viperine snake (Natrix maura) on Mallorca. Biodivers Conserv 15:3045–3054. doi: 10.1007/s10531-005-4878-y CrossRefGoogle Scholar
  24. Guijarro JA (2002) Valores horarios medios de temperatura y humedad relativa en Baleares. Bol Mens Climatol 57:121–134Google Scholar
  25. Herrel A, Huygue K, Vanhooydonck B, Backeljau T, Breuguelmans K, Grbac I, Van Damme R, Irschick DJ (2008) Rapid large-scale evolutionary divergence in morphology and performance associated with exploitation of a different dietary resource. Proc Natl Acad Sci 105:4792–4795. doi: 10.1073/pnas.0711998105 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis. Springer, New YorkCrossRefGoogle Scholar
  27. Lillywhite HB, de Delva P, Noonan BP (2002) Patterns of gut passage time and the chronic retention of fecal mass in viperid snakes. In: Schuett GW, Höggren M, Greene HW (eds) Biology of the vipers. Biological Sciences Press, Traverse City, pp. 497–506Google Scholar
  28. Liu H, Stiling P (2006) Testing the enemy release hypothesis: a review and meta-analysis. Biol Invasions 8:1535–1545. doi: 10.1007/s10530-005-5845-y CrossRefGoogle Scholar
  29. Liu X, Li X, Liu Z, Tingley R, Kraus F, Guo Z, Li Y (2014) Congener diversity, topographic heterogeneity and human-assisted dispersal predict spread rates of alien herpetofauna at a global scale. Ecol Lett 17:821–829. doi: 10.1111/ele.12286 CrossRefPubMedGoogle Scholar
  30. Luiselli L, Capula M, Rugiero L, Salvi D, Akani GC (2012) Does interspecific competition with a stronger competitor explains the rarity of an endangered snake on a Mediterranean island? Ecol Res 27:649–655. doi: 10.1007/s11284-012-0936-6 CrossRefGoogle Scholar
  31. Luiselli L, Petrozzi F, Mebert K, Zuffi MA, Amori G (2015) Resource partitioning and dwarfism patterns between sympatric snakes in a micro-insular Mediterranean environment. Ecol Res 30:527–535. doi: 10.1007/s11284-015-1250-x
  32. Martínez-Morales MA, Cuaron AD (1999) Boa constrictor, an introduced predator threatening the endemic fauna on Cozumel Island, Mexico. Biodivers and Conserv 8:957–963. doi: 10.1023/A:1008815004072 CrossRefGoogle Scholar
  33. Mateo JA, Ayres C, López-Jurado LF (2011) Los anfíbios y reptiles naturalizados en España: Historia y evolución de una problemática creciente. Bol Asoc Herpetol Esp 22:1–41Google Scholar
  34. Montes EM, Estarellas J, Ayllón E, Carretero MÁ, Feriche M, Hernández PL, Pleguezuelos JM (2015) Dades preliminars del projecte pilot de control de serps a l’illa d’Eivissa. Monogr Soc Hist Nat Balear 20:443–452Google Scholar
  35. Monzón-Argüello C, Patiño-Martínez C, Christiansen F, Gallo-Barneto R, Cabrera-Pérez MA, Peña-Estevez MA, López-Jurado LF, Lee P (2015) Snakes on an island: independent introductions have different potentials for invasion. Conserv Genet 16:1225–1241. doi: 10.1007/s10592-015-0734-0 CrossRefGoogle Scholar
  36. Pafilis P, Foufopoulos J, Sagonas K, Runemark A, Svensson E, Valakos ED (2011) Reproductive biology of insular reptiles: marine subsidies modulate expression of the island syndrome. Copeia 2011:545–552. doi: 10.1643/CE-10-041 CrossRefGoogle Scholar
  37. Paolucci EM, MacIsaac HJ, Ricciardi A (2013) Origin matters: alien consumers inflict greater damage on prey populations than do native consumers. Divers Distrib 19:988–995. doi: 10.1111/ddi.12073 CrossRefGoogle Scholar
  38. Pérez-Mellado V (2009) Les Sargantanes de les Balears. Documenta Balear, S.L., Palma de MallorcaGoogle Scholar
  39. Pérez-Méndez N, Jordano P, García C, Valido A (2016) The signatures of Anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci Rep 6:24820. doi: 10.1038/srep24820 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Pinya S, Carretero MÁ (2011) The Balearic herpetofauna: a species update and a review on the evidence. Acta Herpetol 6:59–80. doi: 10.13128/Acta_Herpetol-9579 Google Scholar
  41. Pleguezuelos JM, Fahd S (2004) Body size, diet and reproductive ecology of Coluber hippocrepis in the Rif (northern Morocco). Amphib-Reptil 25:287–302CrossRefGoogle Scholar
  42. Pleguezuelos JM, Feriche M (1999) Reproductive ecology of the horseshoe whip snake (Coluber hippocrepis) in the Iberian peninsula. J Herpetol 33:202–207CrossRefGoogle Scholar
  43. Pleguezuelos JM, Feriche M (2014) Hemorrhois hippocrepis (Linnaeus, 1758). In: Ramos MA (ed) Salvador A (coord) Fauna Iberica, vol. 10, MNCN, CSIC, Madrid, pp 722–738. doi:  10.1163/1568538041975099
  44. Pleguezuelos JM, Moreno M (1990) Alimentación de Coluber hippocrepis en el SE de la Península Ibérica. Amphib-Reptil 11:325–337CrossRefGoogle Scholar
  45. Riera N, Traveset A, García O (2002) Breakage of mutualisms by exotic species: the case of Cneorum tricoccon L. in the Balearic islands (western Mediterranean Sea). J Biogeogr 29:713–719. doi: 10.1046/j.1365-2699.2002.00719.x CrossRefGoogle Scholar
  46. Riofrío-Lazo M, Páez-Rosas D (2015) Feeding habits of introduced black rats, Rattus rattus, in nesting colonies of Galapagos petrel on San Cristóbal Island. Galapagos PLoS ONE. doi: 10.1371/journal.pone.0127901 PubMedGoogle Scholar
  47. Salvador A (coord.) (2014) Reptiles. Fauna Ibérica, vol. X. MNCN, CSIC, MadridGoogle Scholar
  48. Santos X, Feriche M, León R, Filippakopoulou A, Vidal-García M, Llorente GA, Pleguezuelos JM (2011) Tail breakage frequency as an indicator of predation risk for the aquatic snake Natrix maura. Amphib-Reptil 32:375–383CrossRefGoogle Scholar
  49. Santos X, Llorente GA (2004) Lipid dynamics in the viperine snake Natrix maura from the Ebro Delta. Oikos 105:132–140. doi: 10.1163/017353711X587264 CrossRefGoogle Scholar
  50. Secor SM (2003) Gastric function and its contribution to the postprandial metabolic response of the Burmese python Python molurus. J Exp Biol 206:1621–1630. doi: 10.1242/jeb.00300 CrossRefPubMedGoogle Scholar
  51. Secor SM, Diamond J (1997) Determinants of post-feeding metabolic response in Burmese pythons, Python molurus. Physiol Zool 70:202–212. doi: 10.2307/30164303 CrossRefPubMedGoogle Scholar
  52. Shine R (1987) Ecological comparisons of island and mainland populations of Australian tigersnakes (Notechis: Elapidae). Herpetol 43:233–240Google Scholar
  53. Silva-Rocha I, Salvi D, Sillero N, Mateo JA, Carretero MÁ (2015) Snakes on the Balearic islands: an invasion tale with implications for native biodiversity conservation. PLoS One. doi: 10.1371/journal.pone.0121026 Google Scholar
  54. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32. doi: 10.1023/A:1010086329619
  55. Simberloff D, Martin JL, Genovesi P, Maris V, Wardle DA, Aronson J, Courchamp F, Galil B, García-Berthou E, Pascal M, Pysek P, Sousa R, Tabacchi E, Vilà M (2013) Impacts of biological invasions: what’s what and the way forward. TREE 28:58–66PubMedGoogle Scholar
  56. Teerink BJ (2004) Hair of West European mammals: atlas and identification key. Cambridge Univ Press, CambridgeGoogle Scholar
  57. Wang T, Morten Z, Arvedsen S, Vedel-Smith C, Overgaard J (2003) Effects of temperature on the metabolic response to feeding in Python molurus. Comp Biochem Physiol A 133:519–527. doi: 10.1016/S1095-6433(02)00250-7 CrossRefGoogle Scholar
  58. Waye HL, Mason RT (2008) A combination of body condition measurements is more informative than conventional condition indices: temporal variation in body condition and corticosterone in brown tree snakes (Boiga irregularis). Gen Comp Endocr 155:607–612CrossRefPubMedGoogle Scholar
  59. Whittaker RJ, Fernández-Palacios JM (2007) Island Biogeography: Ecology, Evolution, and Conservation. Oxford Univ Press, OxfordGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Arlo Hinckley
    • 1
  • Elba Montes
    • 2
  • Enrique Ayllón
    • 3
  • Juan M Pleguezuelos
    • 4
    Email author
  1. 1.Estación Biológica de Doñana (EBD-CSIC), Conservation and Evolutionary Genetics GroupSevillaSpain
  2. 2.Department of EnvironmentIbiza Island CouncilIbizaSpain
  3. 3.Asociación Herpetológica EspañolaLeganés MadridSpain
  4. 4.Departamento de Zoología, Facultad de CienciasUniversidad de GranadaGranadaSpain

Personalised recommendations