Skip to main content

Advertisement

Log in

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

  • Original Article
  • Published:
European Journal of Wildlife Research Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • 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 Mallorca

  • 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 135:109–118

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. 87–115

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

  • Ayllón E (2015) La culebra de herradura (Hemorrhois hippocrepis) en las islas Baleares. Bol Asoc Herpetol Esp 26:88–91

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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. 483–495

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Capula M (1994) Population genetics of a colonizing lizard: loss of variability in introduced populations of Podarcis sicula. Experientia 50:691–696

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Cattaneo A (2015) Contributo alla conoscenza dei serpenti delle isole del canale di Sicilia. Naturalista Siciliano S IV 34:3–28

    Google Scholar 

  • 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. 397–429

    Google Scholar 

  • Clevenger AP (1993) Pine marten (Martes martes Linné, 1758) comparative feeding ecology in an island and mainland population of Spain. Z Saugetierkd 58:212–212

    Google Scholar 

  • Close DA, Fitzpatrick MS, Li HW (2002) The ecological and cultural importance of a species at risk of extinction, Pacific lamprey. Fisheries 27:19–25

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gosàlbez J (1987) Insectívors i rosegadors de Catalunya. Ketres, Barcelona

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Guijarro JA (2002) Valores horarios medios de temperatura y humedad relativa en Baleares. Bol Mens Climatol 57:121–134

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraus F (2009) Alien reptiles and amphibians: a scientific compendium and analysis. Springer, New York

    Book  Google Scholar 

  • 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. 497–506

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

  • 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

    Article  Google Scholar 

  • 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 22:1–41

    Google Scholar 

  • 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 20:443–452

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Pérez-Mellado V (2009) Les Sargantanes de les Balears. Documenta Balear, S.L., Palma de Mallorca

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 

  • Pleguezuelos JM, Fahd S (2004) Body size, diet and reproductive ecology of Coluber hippocrepis in the Rif (northern Morocco). Amphib-Reptil 25:287–302

    Article  Google Scholar 

  • Pleguezuelos JM, Feriche M (1999) Reproductive ecology of the horseshoe whip snake (Coluber hippocrepis) in the Iberian peninsula. J Herpetol 33:202–207

    Article  Google Scholar 

  • 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

  • Pleguezuelos JM, Moreno M (1990) Alimentación de Coluber hippocrepis en el SE de la Península Ibérica. Amphib-Reptil 11:325–337

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Salvador A (coord.) (2014) Reptiles. Fauna Ibérica, vol. X. MNCN, CSIC, Madrid

  • 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 32:375–383

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Shine R (1987) Ecological comparisons of island and mainland populations of Australian tigersnakes (Notechis: Elapidae). Herpetol 43:233–240

    Google Scholar 

  • 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 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32. doi:10.1023/A:1010086329619

  • 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 28:58–66

    PubMed  Google Scholar 

  • Teerink BJ (2004) Hair of West European mammals: atlas and identification key. Cambridge Univ Press, Cambridge

  • 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

    Article  Google Scholar 

  • 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 155:607–612

    Article  CAS  PubMed  Google Scholar 

  • Whittaker RJ, Fernández-Palacios JM (2007) Island Biogeography: Ecology, Evolution, and Conservation. Oxford Univ Press, Oxford

Download references

Acknowledgements

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan M Pleguezuelos.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hinckley, A., Montes, E., Ayllón, E. et al. 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 . Eur J Wildl Res 63, 13 (2017). https://doi.org/10.1007/s10344-016-1068-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10344-016-1068-z

Keywords

Navigation