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Effect of exotic mammalian predators on parasites of Cory's shearwater: ecological effect on population health and breeding success

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Abstract

Predator activity around the nests induces stress in breeding birds, which may have weaker immunity and are therefore more susceptible to parasite infections. The influence of predators on parasites has only been observed in land birds, and most studies are experimental. As seabird colonies offer excellent conditions for parasites, here we assess the influence of mouse, rat, and cat activity on parasites in Cory's shearwater (Calonectris diomedea borealis). Adults were examined for blood parasites and one adult and the juvenile from 53 nests were inspected for ectoparasites over two consecutive years (2010 and 2011). Nests differed in their physical characteristics and indices of mammal predator activity and were checked weekly to assess breeding success. Our results showed absence of blood parasites. Among the environmental factors, predator pressure received the most support (89 %) from the data as influencing nest ectoparasite intensity. Birds most infected had worse body condition, and breeding success was negatively influenced by predator activity and ectoparasite intensity. To our knowledge, this is the first analysis of the interaction between mammal predators and ectoparasites in seabird species and supports greater protection through eradication efforts. In addition, we provide the first data on the endoparasite fauna of Cory's shearwater.

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References

  • Aguirre-Muñoz A, Croll DA, Donlan CJ, Henry RW, Hermosillo MA, Howald GR, Keitt BS, Luna-Mendoza L, Rodríguez-Malagón M, Salas-Flores LM, Samaniego-Herrera A, Sanchez-Pacheco JA, Sheppard J, Tershy BR, Toro-Benito J, Wolf S, Wood B (2009) High-impact conservation: invasive mammal eradications from the islands of Western México. Ambio 37(2):101–107 doi:10.1579/0044-7447(2008)37[101:hcimef]2.0.co;2

    Google Scholar 

  • Anderson R (1979) The influence of parasitic infection on the dynamics of host population growth. In: Anderson RM, Turner BD, Taylor LR (eds) Population dynamics. Blackwell Scientific Publications, Oxford, London, UK

  • Anderson RC, Chabaud AG, Willmott S (1974) CIH Keys to the nematode parasites of vertebrates, vol 1. Commonwealth Institute of Helminthology, Farnham Royal, UK

    Google Scholar 

  • Ash JS (1960) A study of the Mallophaga of birds with particular reference to their ecology. Ibis 102(1):93–110

    Google Scholar 

  • Atkinson CT, Van Riper CI (1991) Pathogenicity and epizootiology of avian haematozoa: plasmodium, leucocytozoon, and haemoproteus. In: Loye JE, Zuk M (eds) Oxford University Press Oxford, UK

  • Baer JG (1954) Revision taxinomique et étude biologique des Cestodes de la famille des Tetrabothriidae: parasites d'oiseaux de haute mer et de mammifères marins. Mémoires de l'Université de Neuchatel, Série inquarto 1:1–121

    Google Scholar 

  • Beaucournu JC, Degeilh B, Guiguen C (2005) Bird fleas (Insecta: Siphonaptera): taxonomic diversity, biogeographical distribution. Parasite 12(2):111–121

    Google Scholar 

  • Bell G (1980) The costs of reproduction and their consequences. Am Nat 116(1):45–76

    Google Scholar 

  • Bonnaud E, Bourgeois K, Vidal E, Legrand J, Le Corre M (2009) How can the Yelkouan shearwater survive feral cat predation? A meta-population structure as a solution? Popul Ecol 51(2):261–270. doi:10.1007/s10144-008-0134-0

    Article  Google Scholar 

  • Booth DT, Clayton DH, Block BA (1993) Experimental demonstration of the energetic cost of parasitism in free-ranging hosts. Proc Roy Soc London Ser B Biol Sci 253(1337):125–129

    Google Scholar 

  • Bosch M, Torres J, Figuerola J (2000) A helminth community in breeding Yellow-legged Gulls (Larus cachinnans): pattern of association and its effect on host fitness. Can J Zool 78(5):777–786

    Google Scholar 

  • Boulinier T, Danchin E (1996) Population trends in kittiwake (Rissa tridactyla) colonies in relation to tick infestation. Ibis 138(2):326–334

    Article  Google Scholar 

  • Bretagnolle V, Lequette B (1990) Structural variation in the call of the Cory’s Shearwater (Calonectris diomedea, Aves, Procellariidae). Ethol 85(4):313–323

    Google Scholar 

  • Brooke M (2004) Albatrosses and petrels across the world. Oxford University Press, USA

    Google Scholar 

  • Brooke MD, Hilton GM, Martins TLF (2007) The complexities of costing eradications: a reply to Donlan & Wilcox. Anim Conserv 10(2):157–158. doi:10.1111/j.1469-1795.2007.00107.x

    Article  Google Scholar 

  • Brown CR, Brown MB, Rannala B (1995) Ectoparasites reduce long-term survival of their avian host. Proc Roy Soc London Ser B Biol Sci 262(1365):313–319

    Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, New York

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J. parasitol 83(4):575–583

    Google Scholar 

  • Capizzi D, Baccetti N, Sposimo P (2010) Prioritizing rat eradication on islands by cost and effectiveness to protect nesting seabirds. Biol Conserv 143(7):1716–1727

    Article  Google Scholar 

  • Chapman BR, George JE (1991) The effects of ectoparasites on cliff swallow growth and survival. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution, and behaviour. Oxford University Press, USA

  • Clayton DH (1991) Coevolution of avian grooming and ectoparasite avoidance. In: Loye JE, Zuk M (eds) Bird-parasite interactions: ecology, evolution, and behaviour. Oxford University Press, USA

  • Clayton DH, Tompkins DM (1995) Comparative effects of mites and lice on the reproductive success of rock doves (Columba livia). Parasitol 110(2):195–195

    Google Scholar 

  • Clifford CM (1979) Tick-borne viruses of seabirds. In: Kurstak E (ed) Arctic and tropical arboviruses. Academic Press, London, UK

    Google Scholar 

  • Clinchy M, Zanette L, Boonstra R, Wingfield JC, Smith JNM (2004) Balancing food and predator pressure induces chronic stress in songbirds. Proceedings of the Royal Society of London Series B. Biol Sci 271(1556):2473–2479

    Google Scholar 

  • Cordeiro A (1717) Historia Insulana das Ilhas a Portugal Sugeytas no Oceano Occidental. Lisboa, ed. 1981. Secretaria Regional da Educação e Cultura, Angra de Heroísmo, Azores

  • Daoust PY, Conboy G, McBurney S, Burgess N (1998) Interactive mortality factors in common loons from Maritime Canada. J Wildl Dis 34(3):524–531

    PubMed  CAS  Google Scholar 

  • Dyer GW, Williams HE, Mignucci-Giannoni AA, Jiménez-Marrero MN, Bunkley-Williams L, Moore PD, Pence BD (2002) Helminth and arthropod parasites of the brown pelican, Pelecanus occidentalis, in Puerto Rico, with a compilation of all metazoan parasites reported from this host in the Western Hemisphere. Avi Pathol 31(5):441–448

    Google Scholar 

  • Esparza B, Martínez-Abraín A, Merino S, Oro D (2004) Brief report Immunocompetence and the prevalence of haematozoan parasites in two longlived seabirds. Orn Fenn 81:00–00

    Google Scholar 

  • Estrada-Peña A, Martinez JM, Sanchez Acedo C, Quilez J, Del Cacho E (2004) Phenology of the tick, Ixodes ricinus, in its southern distribution range (central Spain). Medical and Vet Entomol 18(4):387–397

  • Festa-Bianchet M (1989) Individual differences, parasites, and the costs of reproduction for bighorn ewes (Ovis canadensis). J Anim Ecol 58(3):785–795

    Google Scholar 

  • Forero MG, González-Solis J, Igual JM, Hobson KA, Ruíz X, Viscor G (2006) Ecological and physiological variance in T-cell mediated immune response in Cory's shearwaters. Condor 108(4):865–876

    Article  Google Scholar 

  • Forrester SG, Lankester MW (1997) Extracting protostrongylid nematode larvae from ungulate feces. J Wildl Dis 33(3):511–516

    Google Scholar 

  • Foster GW, Kinsella JM, Price RD, Mertins JW, Forrester DJ (1996) Parasitic helminths and arthropods of Greater Shearwaters (Puffinus gravis) from Florida. J Helminthol Soc Washington 63(1):83–88

    Google Scholar 

  • Galaktionov K, Bustnes JO (1996) Diversity and prevalence of seabird parasites in intertidal zones of the southern Barents Sea coast. NINA-NIKU project report, SN - 9788242606877. Foundation for Nature Research and Cultural Heritage Research. http://books.google.com.ph/books?id=JxVkMwEACAAJ

  • Gómez-Díaz E, Navarro J, González-Solís J (2008) Ectoparasite community structure on three closely related seabird hosts: a multiscale approach combining ecological and genetic data. Ecography 31(4):477–489

    Google Scholar 

  • Gonzáles-Solís J, Abella JC (1997) Negative record of haematozoan parasites on Cory's shearwater Calonectris diomedea. Orn Fenn 74:153–155

    Google Scholar 

  • Granadeiro JP (1991) The breeding biology of Cory's Shearwater Calonectris diomedea borealis on Berlenga Island, Portugal. Seabird 13:30–39

    Google Scholar 

  • Granadeiro JP (1993) Variation in measurements of Cory’s Shearwater between populations and sexing by discriminant analysis. Ring Mig 14(2):103–112

    Google Scholar 

  • Gray JS (2002) Biology of Ixodes species ticks in relation to tick-borne zoonoses. Wien Klin Wochenschrift 114(13–14):473

    Google Scholar 

  • Gustafsson L, Nordling D, Andersson M, Sheldon B, Qvarnstrom A (1994) Infectious diseases, reproductive effort and the cost of reproduction in birds. Phil Trans Roy Soc London Ser B Biol Sci 346(1317):323–331

    Google Scholar 

  • Hervías S, Henriques A, Oliveira N, Pipa T, Cowen H, Ramos JA, Nogales M, Geraldes P, Silva C, Ibáñez R, Oppel S (2013) Studying the effects of multiple invasive mammals on Cory's shearwater nest survival. Biol Invasions 15(1):143–155. doi:10.1007/s10530-012-0274-1

    Article  Google Scholar 

  • Hervías S, Silva C, Pipa T, Oliveira N, Henriques A, Geraldes PL, Mealha S, Diaz E, Bravo I, Oppel S, Medina FM (2012) Invasive mammal species on Corvo Island: is their eradication technically feasible? Airo 22:12–28

    Google Scholar 

  • Hoberg EP, Ryan PG (1989) Ecology of helminth parasitism in Puffinus gravis (Procellariiformes) on the breeding grounds at Gough Island. Can J Zool 67(1):220–225

    Google Scholar 

  • Holmes JC, Bethel WM (1972) Modification of intermediate host behaviour by parasites. Zool J Linn Soc 51:123–149

    Google Scholar 

  • Hudson PJ, Dobson AP, Newborn D (1992) Do parasites make prey vulnerable to predation? Red grouse and parasites. J Anim Ecol 61(3):681–692

    Google Scholar 

  • Hurtrez-Boussès S, Perret P, Renaud F, Blondel J (1997) High blowfly parasitic loads affect breeding success in a Mediterranean population of blue tits. Oecol 112(4):514–517

    Google Scholar 

  • Jones EK, Clifford CM, Keirans JE, Kohls GM (1972) The ticks of Venezuela (Acarina: Ixodoidea) with a key to the species of Amblyomma in the Western Hemisphere. Brigham Young Univ Sci Bull Biol ser 17(4):1–40

    Google Scholar 

  • Jones HP, Tershy BR, Zavaleta ES, Croll DA, Keitt B, Finkelstein ME, Howald GR (2008) Severity of the effects of invasive rats on seabirds: a global review. Conserv Biol 22(1):16–26. doi:10.1111/j.1523-1739.2007.00859.x

    Article  PubMed  Google Scholar 

  • Krants G (1978) A manual of acarology, 2nd edn. Oregon State University Book Stores Inc., Oregon, USA

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) Effect or air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38(5):629–637

    Article  PubMed  CAS  Google Scholar 

  • Lee PLM, Clayton DH (1995) Population biology of swift (Apus apus) ectoparasites in relation to host reproductive success. Ecol Entomol 20(1):43–50

    Article  Google Scholar 

  • Little RM, Earlé RA (1994) Lack of avian haematozoa in the Phasianinae of Robben Island. Ostrich 65:343–344

    Google Scholar 

  • Loye JE, Carroll SP (1998) Ectoparasite behavior and its effects on avian nest site selection. Ann Entomol Soc Am 91(2):159–163

    Google Scholar 

  • Marcogliese DJ (2005) Parasites of the superorganism: Are they indicators of ecosystem health? Inter J Parasitol 35(7):705–716

    Google Scholar 

  • Marshall AG (1981) The ecology of ectoparasitic insects. Academic Press, London

    Google Scholar 

  • Martínez-Abraín A, Esparza B, Oro D (2004) Lack of blood parasites in bird species: does absence of blood parasite vectors explain it all. Ardeola 51(1):225–232

    Google Scholar 

  • McCoy KD, Boulinier T, Schad GA, Schjørring S, Michalakis Y (2002) Local adaptation of the ectoparasite Ixodes uriae to its seabird host. Evol Ecol Res 4(3):441–456

    Google Scholar 

  • Merino S, Mínguez E (1998) Absence of haematozoa in a breeding colony of the Storm Petrel Hydrobates pelagicus. Ibis 140(1):180–181

    Google Scholar 

  • Merino S, Mínguez E, Belliure B (1999) Ectoparasite effects on nestling European storm-petrels. Waterbirds 22(2):297–301

    Google Scholar 

  • Mifsud N, Purcell A, Chen W, Holdsworth R, Tait B, McCluskey J (2008) Immunodominance hierarchies and gender bias in direct TCD8-cell alloreactivity. Am J Transplant 8(1):121–132

    Article  PubMed  CAS  Google Scholar 

  • Møller AP (1997) Developmental stability and fitness: a review. Oxford University Press, Oxford

    Google Scholar 

  • Møller AP, Nielsen JT (2007) Malaria and risk of predation: a comparative study of birds. Ecol 88(4):871–881

    Google Scholar 

  • Monteiro LR, Ramos JA, Furness RW (1996) Past and present status and conservation of the seabirds breeding in the Azores Archipelago. Biol Conserv 78(3):319–328

    Article  Google Scholar 

  • Moss R, Trenholm I, Watson A, Parr R (1990) Parasitism, predation and survival of hen red grouse Lagopus lagopus scoticus in spring. J Anim Ecol 59:631–642

    Google Scholar 

  • Moyer BR, Drown DM, Clayton DH (2002) Low humidity reduces ectoparasite pressure: implications for host life history evolution. Oikos 97(2):223–228

    Article  Google Scholar 

  • Muzaffar S, Jones I (2004) Parasites and diseases of the auks (Alcidae) of the world and their ecology—a review. Mar Ornithol 32(2)

  • Oppel S, Beaven B, Bolton M, Vickery JA, Bodey TW (2011) Eradication of invasive mammals on islands inhabited by humans and domestic animals. Conserv Biol 25(2):232–240. doi:10.1111/j.1523-1739.2010.01601.x

    PubMed  Google Scholar 

  • Oppliger A, Christe P, Richner H (1996) Clutch size and malaria resistance. Nature 381(6583):565

    Article  PubMed  CAS  Google Scholar 

  • Packer C, Holt RD, Hudson PJ, Lafferty KD, Dobson AP (2003) Keeping the herds healthy and alert: implications of predator control for infectious disease. Ecol Lett 6(9):797–802

    Google Scholar 

  • Paltridge R (2002) The diets of cats, foxes and dingoes in relation to prey availability in the Tanami Desert, Northern Territory. Wildl Res 29(4):389–403

    Article  Google Scholar 

  • Pemberton RT (1963) Helminth Parasites of Three Species of British Gulls, Larus argentatus Pont., L. fuscus L. and L. ridibundus L. J Helminthol 37(1–2):57–88

  • Pereira C (2000) Aves dos Açores. Portuguese Society for the Protection of Birds. Lisboa, Portugal

    Google Scholar 

  • Pravosudov VV (2006) On seasonality in food-storing behaviour in parids: do we know the whole story? Anim Behav 71:1455–1460

    Article  Google Scholar 

  • Price RD, Clay T (1972) A review of the genus Austromenopon (Mallophaga: Menoponidae) from the Procellariiformes. Annals of the Entomological Society of America 65(2):487–504

  • Price R, Hellenthal R, Palma R, Johnson K, Clayton D (2004) The chewing lice: world checklist and biological overview. Syst Biol 53(4):666–668

    Article  Google Scholar 

  • Pritchard MH, Kruse GOW (1982) The collection and preservation of animal parasites. University of Nebraska Press, Lincoln

    Google Scholar 

  • Development Core Team R (2010) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Raouf SA, Smith LC, Brown MB, Wingfield JC, Brown CR (2006) Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim Behav 71(1):39–48

    Google Scholar 

  • Ramos JA, Bowler J, Davis L, Venis S, Quinn J, Middleton C (2001) Activity patterns and effect of ticks on growth and survival of tropical Roseate Tern nestlings. The Auk 118(3):709–716

    Google Scholar 

  • Ramos JA, Moniz Z, Solá E, Monteiro LR (2003) Reproductive measures and chick provisioning of Cory's Shearwater Calonectris diomedea borealis in the Azores: timing of breeding influenced wing-length at fledging, and egg size may be an indicator of fledging weight and the amount of food received by chicks. Bird Study 50(1):47–54

    Article  Google Scholar 

  • Restrepo C, Vitousek P (2001) Landslides, alien species, and the diversity of a Hawaiian Montane Mesic Ecosystem. Biotropica 33(3):409–420

    Google Scholar 

  • Rodrigues P, Cunha RTD (2012) Birds as a tool for island habitat conservation and management. Am J Environ Sci 8:5–10

    Article  Google Scholar 

  • Sagar PM, Horning DS (1998) Mass-related survival of fledgling sooty shearwaters Puffinus griseus at the Snares, New Zealand. Ibis 140(2):329–331

  • Santana F, Martín A, Nogales M (1986) Datos sobre la alimentación del gato cimarrón (Felis catus Linnaeus, 1758) en los montes de Pajonales, Ojeda e Inagua (Gran Canaria). Vieraea 16:113–117

    Google Scholar 

  • Sarmento PB, Cruz JP, Eira CI, Fonseca C (2010) Habitat selection and abundance of common genets Genetta genetta using camera capture-mark-recapture data. Eur J Wildl Res 56:59–66. doi:10.1007/s10344-009-0294-z

    Article  Google Scholar 

  • Skrjabin K, Shikhobalova N, Mozgovoi A (1951) Key to parasitic nematodes, vol 2. Oxyurata and Ascaridata. Izdatel'stvo Akademii Nauk SSSR, Moscow. Russia English translation by Amerind Publishing Co Pvt Ltd, New Delhi, India, 1982

    Google Scholar 

  • Temple S (1987) Do predators always capture substandard individuals disproportionately from prey populations? Ecol 68(3):669–674

    Google Scholar 

  • Thomas M (1999) Feasibility of using wax-blocks to measure rodent and possum abundance and changes in population size. In: Conservation D (ed) Progress in mammal pest control on New Zealand conservation lands, Science for Conservation 127. Christchurch, New Zealand, pp 39–48

    Google Scholar 

  • Towns D (2009) Eradications as reverse invasions: lessons from Pacific rat (Rattus exulans) removals on New Zealand islands. Biol Invasions 11(7):1719–1733

    Article  Google Scholar 

  • Veitch CR, Clout MN, Towns DR (2011) Island invasives: eradication and management. The International Union for Conservation of Nature, Gland, Switzerland

  • Vermeil C, Marguet S (1967) Sur le diagnostic des larves d’ornithodores du complexe coniceps-capensis (Acarina: Argasidae) Ornithodoros coniceps (Canestrini 1890) maritimus n. ssp. prevaut dans les lles de basse Bretagne. Acarologia 9:557–565

  • Yamaguti S (1971) Synopsis of digenetic trematodes of vertebrates. Keigaku Pub. Co., Tokyo

    Google Scholar 

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Acknowledgments

his study was made possible by LIFE07 NAT/P/000649 ‘Safe Islands for Seabirds’, coordinated by the Portuguese Society for the Study of Birds (SPEA) and co-financed by the European Union Commission. We thank P. Domingos, E. Díaz, F. Ceia, R. Ceia, S. Oppel, H. Cowen, T. Pipa, J. Benedicto, M. Goh and the Life Project team and volunteers for invaluable field help. We appreciate the input of J. Díaz, L. Chitimia and M. Kinsella who contributed to the identification of ticks and endoparasites. We are also grateful for the permission (no. 84; 2011) given by Direcção Regional do Ambiente (Horta, Portugal) for handling wildlife. The authors declare that all experiments described in this study complied with the current laws of Portugal.

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Hervías, S., Ramos, J.A., Nogales, M. et al. Effect of exotic mammalian predators on parasites of Cory's shearwater: ecological effect on population health and breeding success. Parasitol Res 112, 2721–2730 (2013). https://doi.org/10.1007/s00436-013-3443-y

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