Skip to main content

Advertisement

Log in

Behavioural plasticity in nest-site selection of a colonial seabird in response to an invasive carnivore

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Non-native invasive species are one of the most serious threats to biodiversity and are considered the leading cause of extinction of several bird taxa, including seabirds. Introduced American mink (Neovison vison) have caused devastating effects on island populations of several colonial seabird species. In this study, we investigated the direct and indirect effects of mink on population dynamics and reproductive success of European shags (Phalacrocorax aristotelis) breeding at Illas Cíes, one of the most important colonies of the species in Southern Europe. A severe episode of mink predation on adult shags occurred in the year when mink arrived in the breeding colonies, though the number of shags killed dropped abruptly in subsequent years. We found that, after the arrival of mink, shags moved to nest-sites that afforded greater protection from carnivores. This shift caused a substantial reduction in mortality by predation, but probably entailed a cost in terms of their reproductive success because sites with lower levels of predation risk showed a higher risk of egg loss by nest flooding due to poorer drainage. Our study highlights that behavioural plasticity may allow shags to cope with invasive predators.

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
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aebischer NJ (1986) Retrospective investigation of an ecological disaster in the shag, Phalacrocorax aristotelis: a general method based on long-term marking. J Anim Ecol 55:613–629

    Article  Google Scholar 

  • Aebischer NJ, Wanless S (1992) Relationships between colony size, adult non-breeding and environmental conditions for Shags Phalacrocorax aristotelis on the Isle of May, Scotland. Bird Study 39:43–52

    Article  Google Scholar 

  • Barros A, Álvarez D, Velando A (2013) Cormorán moñudo—Phalacrocorax aristotelis. In: Salvador A, Morales MB (eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org. Accessed 24 June 2015

  • Barros A, Álvarez D, Velando A (2014) Long-term reproductive impairment in a seabird after the Prestige oil spill. Biol Lett. doi:10.1098/rsbl.2013.1041

    PubMed  PubMed Central  Google Scholar 

  • Bennett PM, Owens IPF (1997) Variation in extinction risk among birds: chance or evolutionary predisposition? Proc R Soc Lond B 264:401–408

    Article  Google Scholar 

  • BirdLife International (2000) Threatened birds of the world. Lynx Edicions and BirdLife International, Barcelona

    Google Scholar 

  • Bixler KS (2010) Why aren’t Pigeon Guillemots in Prince William Sound, Alaska, recovering from the Exxon Valdez oil spill? M.Sc. Thesis, Oregon State University, Corvallis, Oregon

  • Björsson TE, Heirstensson P (1991) Mink in southern Breidfjordur Bay. In: Macdonald D, Strachan R (eds) The mink and the water vole. Analyses for Conservation 7. Wildlife Conservation Research Unit and the Environment Agency, Oxford, pp 3–12

    Google Scholar 

  • Blackburn TM, Cassey P, Duncan RP, Evans KL, Gaston KJ (2004) Avian extinction and mammalian introductions on oceanic islands. Science 305:1955–1958

    Article  CAS  PubMed  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Bonesi L, Macdonald DW (2004) Evaluation of sign surveys as a way to estimate the relative abundance of American mink (Mustela vison). J Zool 262:65–72

    Article  Google Scholar 

  • Bonesi L, Palazón S (2007) The American mink in Europe: status, impacts, and control. Biol Conserv 134:470–483

    Article  Google Scholar 

  • Bonesi L, Chanin P, Macdonald W (2004) Competition between Eurasian otter Lutra lutra and American mink Mustela vison probed by niche shift. Oikos 106:19–26

    Article  Google Scholar 

  • Brzeziński M, Natorff M, Zalewski A, Zmihorski M (2012) Numerical and behavioral responses of waterfowl to the invasive American mink: a conservation paradox. Biol Conserv 147:68–78

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. Springer, New York

    Google Scholar 

  • Craik C (1995) Effects of North American mink on the breeding success of terns and smaller gulls in west Scotland. Seabird 17:3–11

    Google Scholar 

  • Craik C (1997) Long-term effects of North American Mink Mustela vison on seabirds in western Scotland. Bird Study 44:303–309

    Article  Google Scholar 

  • Croxall JP, Rothery P (1991) Population regulation of seabirds: implications of their demography for conservation. In: Perrins CM, Lebreton JD, Hirons GJM (eds) Bird population studies, relevance to conservation and management. University Press, Oxford

    Google Scholar 

  • Dunstone N (1993) The mink. T & AD Poyser Ltd, London

    Google Scholar 

  • Eggers S, Griesser M, Nystrand M, Ekman J (2006) Predation risk induces changes in nest-site selection and clutch size in the Siberian jay. Proc R Soc Lond B 273:701–706

    Article  Google Scholar 

  • Fleming MA, Cook JA (2010) MtDNA and microsatellite DNA provide evidence of fur farm ancestry for mink populations in Prince William Sound, Alaska. Exxon Valdez Oil Spill Restoration Project 070853. Museum of Southwestern Biology, University of New Mexico, Albuquerque, NM

  • Folkestad AO (1982) The effect of mink predation on some seabird species. Viltrapport 21:42–49

    Google Scholar 

  • Fontaine JJ, Martin TE (2006) Habitat selection responses of parents to offspring predation risk: an experimental test. Am Nat 168:811–818

    Article  CAS  PubMed  Google Scholar 

  • Forstmeier W, Weiss I (2004) Adaptative plasticity in nest-site selection in response to predation risk. Oikos 104:487–499

    Article  Google Scholar 

  • Furness RW, Monaghan P (1987) Seabird ecology. Blackie, Glasgow

    Google Scholar 

  • García-Díaz P, Lizana M (2013) Reproductive aspects of American minks (Neovison vison) in central Spain: testing the effects of prey availability. Mamm Biol 78:111–117

    Google Scholar 

  • Gobster PH (2005) Invasive species as ecological threat: is restoration an alternative to fear-based resource management? Ecol Rest 23:261–270

    Article  Google Scholar 

  • Harfenist A, Ydenberg RC (1995) Parental provisioning and predation risk in rhinoceros auklets (Cerorhinca monocerata): effects on nestling growth and fledging. Behav Ecol 6:82–86

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Biol 46:10–18

    Google Scholar 

  • Lima SL (2009) Predators and the breeding bird: behavioural and reproductive flexibility under the risk of predation. Biol Rev 84:485–513

    Article  PubMed  Google Scholar 

  • Little RC, Milliken GA, Stroup WW, Wolfinger RD, Schabenberger O (2006) SAS for mixed models, 2nd edn. SAS Institute Inc, Cary

    Google Scholar 

  • Mainwaring MC, Hartley IR, Lambrechts MM, Deeming DC (2014) The design and function of birds’ nests. Ecol Evol 4:3909–3928

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin TE (1993) Nest Predation and nest-sites: new perspectives on old patterns. Bioscience 43:523–532

    Article  Google Scholar 

  • Martínez-Abraín A, Velando A, Oro D, Genovart M, Gerique C, Bartolomé MA, Villuendas E, Sarzo B (2006) Sex-specific mortality of European shags after the Prestige oil spill: demographic implications for the recovery of colonies. Mar Ecol Prog Ser 318:271–276

    Article  Google Scholar 

  • McNeely JA (2005) Human dimensions of invasive alien species. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species: a new synthesis. Island Press, Washington

    Google Scholar 

  • Melero Y, Palazón S (2011) Visón americano—Neovison vison. In: Enciclopedia Virtual de los Vertebrados Españoles. Salvador A, Cassinello J (ed) Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/. Accessed 20 May 2015

  • Mooney HA, Hobbs RJ (2000) Invasive species in a changing world. Island Press, Washington DC

    Google Scholar 

  • Nelson BJ (2006) The pelecaniformes. Oxford University Press, Oxford

    Google Scholar 

  • Nordström M, Högmander J, Laine J, Nummelin J, Laanetu N, Korpimäki E (2003) Effects of feral mink removal on seabirds, waders and passerines on small islands in the Baltic sea. Biol Conserv 109:359–368

    Article  Google Scholar 

  • Opermanis O, Mednis A, Bauga I (2001) Duck nests and predators: interaction, specialisation and possible management. Wildl Biol 7:87–96

    Google Scholar 

  • Oro D, Pradel R, Lebreton JD (1999) The effects of nest predation and food availability on life history traits in Audouin’s gull. Oecologia 118:438–445

    Article  Google Scholar 

  • Pereira P (2006) Estudio de la metodología para el control de la población de visón americano en el archipiélago de Sálvora en el Parque Nacional Islas Atlánticas de Galicia. Parque Nacional Islas Atlánticas de Galicia (unpublished report)

  • Quillfeldt P, Schenk I, McGill RAR, Strange IJ, Masello JF, Gladbach A, Roesch V, Furness RW (2008) Introduced mammals coexist with seabirds at New Island, Falkland Islands: abundance, habitat preferences and stable isotope analysis of diet. Polar Biol 31:333–349

    Article  Google Scholar 

  • Ratcliffe N, Craik C, Helyar A, Roy S, Scott M (2008) Modelling the benefits of American Mink Mustela vison management options for terns in west Scotland. Ibis 150:114–121

    Article  Google Scholar 

  • Regehr HM, Rodway MS, Montevecchi WA (1998) Antipredator benefits of nest-site selection in Black-legged Kittiwakes. Can J Zool 76:910–915

    Article  Google Scholar 

  • Romero R, Piorno V (2012) Plan de control de visón americano (Neovison vison) en el Parque Nacional de las Islas Atlánticas de Galicia. In: Proceedings of the 7th European conference on biological invasions. Pontevedra (Spain)

  • Russell RW (1999) Comparative demography and life history tactics of seabirds: implications for conservation and marine monitoring life in the slow lane. Ecology and conservation of long-lived marine animals. Am Fish Soc Sympos 23:51–76

    Google Scholar 

  • Saether BE, Bakke O (2000) Avian life history variation and contribution of demographic traits to the population growth rate. Ecology 81:642–653

    Article  Google Scholar 

  • Schüttler E, Ibarra JT, Gruber B, Rozzi R, Jax K (2009) Abundance and habitat preferences of the southernmost population of mink: implications for managing a recent island invasion. Biodivers Conserv 19:725–743

    Article  Google Scholar 

  • Short J, Kinnear JE, Robley A (2002) Surplus killing by introduced predators in Australia—evidence for ineffective antipredator adaptations in native prey species? Biol Conserv 103:283–301

    Article  Google Scholar 

  • Travers M, Clinchy M, Zanette L, Boonstra R, Williams TD (2010) Indirect predator effects on clutch size and the cost of egg production. Ecol Lett 13:980–988

    PubMed  Google Scholar 

  • Vidal-Figueroa T, Delibes M (1987) Primeros datos sobre el visón americano (Mustela vison) en el Suroeste de Galicia y Noroeste de Portugal. Ecología 1:145–152

    Google Scholar 

  • Velando A, Álvarez D (2004) Cormorán moñudo, Phalacrocorax aristotelis aristotelis. In: Madroño A, González C, Atienza JC (eds) Libro Rojo de las Aves de España. Dirección General para la Biodiversidad-SEO/BirdLife, Madrid, pp 60–62

    Google Scholar 

  • Velando A, Freire J (2001) Can the central-periphery distribution become general in seabird colonies? Nest spatial pattern in the European Shag. Condor 103:544–554

    Article  Google Scholar 

  • Velando A, Freire J (2002) Population modelling of European shag at their southern limit: conservation implications. Biol Conserv 107:59–69

    Article  Google Scholar 

  • Velando A, Freire J (2003) Nest-site characteristics, occupation and breeding success in the European shag. Waterbirds 26:473–483

    Article  Google Scholar 

  • Velando A, Marquez JC (2002) Predation risk and habitat selection in the inca tern (Larosterna inca). Can J Zool 80:1117–1123

    Article  Google Scholar 

  • Velando A, Munilla I (2008) Plan de Conservación del Cormorán Moñudo en el Parque Nacional de las Islas Atlánticas. Universidade de Vigo, Spain (unpublished report)

  • Velando A, Ortega-Ruano JE, Freire J (1999) Chick mortality in European shag Stictocarbo aristotelis related to food limitations during adverse weather events. Ardea 87:51–59

    Google Scholar 

  • Velando A, Álvarez D, Mouriño J, Arcos F, Barros A (2005a) Population trends and reproductive success of the European shag Phalacrocorax aristotelis on the Iberian Peninsula following the Prestige oil spill. J Ornithol 146:116–120

    Article  Google Scholar 

  • Velando A, Munilla I, Leyenda PM (2005b) Short-term indirect effects of the Prestige oil spill on a marine top predator: changes in prey availability for European shags. Mar Ecol Prog Ser 302:263–274

    Article  Google Scholar 

  • Velando A, Barros A, Moran P (2015) Heterozygosity–fitness correlations in a declining seabird population. Mol Ecol 24:1007–1018

    Article  PubMed  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL, Rejmánek M, Westbrooks R (1997) Introduced species: a significant component of human-caused global change. N Z J Ecol 21:1–16

    Google Scholar 

  • Zuberogoitia I, Zabala J, Martínez JA (2006) Evaluation of sign surveys and trappability of American mink. Consequences for management. Fol Zool 55:257–263

    Google Scholar 

Download references

Acknowledgments

We are grateful to the staff at the Parque Natural Illas Cíes and Parque Nacional Illas Atlánticas de Galicia for logistic support all over the study period, especially to Ramón Nogueira, José Antonio Fernández Bouzas, Vicente Piorno, Susana Torres and Gonzalo Puerto. We are especially grateful to Beatriz Gamallo, Francisco Docampo, Carmen Díaz, Antonio Sampedro, José Manuel Sanchez for their assistance in fieldwork. We thank Alejandro Martinez-Abraín and one anonymous reviewer for their constructive comments, which helped us to improve the manuscript. Permissions were guaranteed by Xunta de Galicia and Parque Nacional Illas Atlánticas de Galicia. Finance was provided by the Spanish Ministerio de Medio Ambiente (Organismo Autónomo Parques Nacionales, 48/2005; 275/2011). Ignacio Munilla was financially supported by an Isidro Parga Pondal fellowship (Xunta de Galicia).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Álvaro Barros.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 363 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Barros, Á., Romero, R., Munilla, I. et al. Behavioural plasticity in nest-site selection of a colonial seabird in response to an invasive carnivore. Biol Invasions 18, 3149–3161 (2016). https://doi.org/10.1007/s10530-016-1205-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-016-1205-3

Keywords

Navigation