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Superpredation patterns in four large European raptors

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Population Ecology

Abstract

Predatory interactions among top predators, like superpredation or intraguild predation (IGP), can influence community structure. Diurnal raptors occupy high trophic levels in terrestrial food webs, and thus can regulate the presence of mesopredators. We studied superpredation (the killing and eating of another predator) in four large European raptors. We gathered 121 dietary studies, totalling 161,456 prey for the Goshawk Accipiter gentilis L., Golden Eagle Aquila chrysaetos L., Bonelli’s Eagle Aquila fasciata Vieillot, and Eagle Owl Bubo bubo L. Results showed that superpredation: (1) is a widespread interaction in large raptors, but it can vary according to the top predator species; (2) is not an important energetic resource for large raptors, but rather seems mostly related to diet diversification when the main prey decreases; (3) is spatially clustered reflecting habitat heterogeneity, but shows no temporal or large-scale spatial trends; and (4) it is associated with lower breeding success of the top predator species. These findings support the food stress hypothesis as the main driving force behind increases in superpredation and IGP in raptors, with the decrease in breeding performance as a side effect. Superpredation by large raptors deserves future research to understand its effects on mesopredators, because on one hand it might contribute to promote biodiversity, while on the other hand, it can sometimes represent an additional risk for small populations of endangered mesopredators.

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References

  • Amarasekare P (2007) Trade-offs, temporal variation, and species coexistence in communities with intraguild predation. Ecology 88:2720–2728. doi:10.1890/06-1515.1

    Article  PubMed  Google Scholar 

  • Amarasekare P (2008) Coexistence of intraguild predators and prey in resource-rich environments. Ecology 89:2786–2797. doi:10.1890/07-1508.1

    Article  PubMed  Google Scholar 

  • Antrop M (2004) Landscape change and the urbanization process in Europe. Landsc Urban Plan 67:9–26. doi:10.1016/S0169-2046(03)00026-4

    Article  Google Scholar 

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564. doi:10.1111/j.1461-0248.2004.00613.x

    Article  Google Scholar 

  • Augustin NH, Mugglestone MA, Buckland ST (1996) An autologistic model for the spatial distribution of wildlife. J Appl Ecol 33:339–347

    Article  Google Scholar 

  • Bivand R (2009) spdep: spatial dependence: weighting schemes, statistics and models. R package version 0.4-34

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2008) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. doi:10.1016/j.tree.2008.10.008

    Article  Google Scholar 

  • Borer ET, Briggs CJ, Holt RD (2007) Predators, parasitoids, and pathogens: a cross-cutting examination of intraguild predation theory. Ecology 88:2681–2688. doi:10.1890/06-1707.1

    Article  PubMed  Google Scholar 

  • Bosch R, Real J, Tintó A, Zozaya EL (2007) An adult male Bonelli’s eagle (Hieraaetus fasciatus) eaten by a subadult golden eagle (Aquila chrysaetos). J Raptor Res 41:338. doi:10.3356/0892-1016(2007)41[338:AAMBEH]2.0.CO;2

    Article  Google Scholar 

  • Cramp S, Simmons KEL, Perrins CM (eds) (1977–1994) The birds of the western palearctic, vol 1–9. Oxford University Press, Oxford

  • Creel S, Christianson D (2008) Relationships between direct predation and risk effects. Trends Ecol Evol 23:194–201. doi:10.1016/j.tree.2007.12.004

    Article  PubMed  Google Scholar 

  • Crooks KC, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566. doi:10.1038/23028

    Article  CAS  Google Scholar 

  • Daugherty MP, Harmon JP, Briggs CJ (2007) Trophic supplements to intraguild predation. Oikos 116:662–677. doi:10.1111/j.0030-1299.2007.15378.x

    Article  Google Scholar 

  • Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R (2008) Key role of European rabbits in the conservation of the Western Mediterranean Basin Hotspot. Conserv Biol 22:1106–1117. doi:10.1111/j.1523-1739.2008.00993.x

    Article  PubMed  Google Scholar 

  • Donázar JA, Hiraldo F, Delibes M, Estrella RR (1989) Comparative food habits of the eagle owl Bubo bubo and the great horned owl Bubo virginianus in six Palearctic and Nearctic biomes. Ornis Scand 20:298–306

    Article  Google Scholar 

  • Dormann C, McPherson J, Araújo M, Bivand R, Bolliger J, Carl G, Davies R, Hirzel A, Jetz W, Kissling W, Kühn I, Ohlemüller R, Peres-Neto P, Reineking B, Schröder B, Schurr F, Wilson R (2007) Methods to account for spatial autocorrelation in the analysis of species distributional data: a review. Ecography 30:609–628. doi:10.1111/j.2007.0906-7590.05171.x

    Article  Google Scholar 

  • Fedriani JM, Fuller TK, Sauvajot RM, York EC (2000) Competition and intraguild predation among three sympatric carnivores. Oecologia 125:258–270. doi:10.1007/s004420000448

    Article  Google Scholar 

  • Fernández C (1993) Effect of the viral haemorrhagic pneumonia of the wild rabbit on the diet and breeding success of the golden eagle. Rev Ecol Terre Vie 48:323–329

    Google Scholar 

  • Ferrer M, Negro JJ (2004) The near extinction of two large European predators: super specialists pay a price. Conserv Biol 18:344–349. doi:10.1111/j.1523-1739.2004.00096.x

    Article  Google Scholar 

  • Gurevitch J, Hedges LV (1999) Statistical issues in ecological meta-analyses. Ecology 80:1142–1149. doi:10.1890/0012-9658(1999)080[1142:SIIEMA]2.0.CO;2

    Article  Google Scholar 

  • Herrera CM (1973) La captura de carnivoros por las strigiformes. Ardeola 19:439–444 (in Spanish with English abstract)

    Google Scholar 

  • Holt RD, Huxel GR (2007) Alternative prey and the dynamics of intraguild predation: theoretical perspectives. Ecology 88:2706–2712. doi:10.1890/06-1525.1

    Article  PubMed  Google Scholar 

  • Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764. doi:10.1086/286018

    Article  Google Scholar 

  • Insley H, Dugan D (1973) Buzzard and golden eagle feeding on other avian predators. Br Birds 66:310–311

    Google Scholar 

  • Ives AR, Cardinale BJ, Snyder WE (2005) A synthesis of subdisciplines: predator-prey interactions, and biodiversity and ecosystem functioning. Ecol Lett 8:102–116. doi:10.1111/j.1461-0248.2004.00698.x

    Article  Google Scholar 

  • Janssen A, Sabelis MW, Magalhães S, Montserrat M, van der Hammen T (2007) Habitat structure affects intraguild predation. Ecology 88:2713–2719. doi:10.1890/06-1408.1

    Article  PubMed  Google Scholar 

  • Järvinen O (1979) Geographical gradients of stability in European land bird communities. Oecologia 38:51–69. doi:10.1007/BF00347824

    Article  Google Scholar 

  • Järvinen O, Ulfstrand S (1980) Species turnover of a continental bird fauna: Northern Europe, 1850–1970. Oecologia 46:186–195. doi:10.1007/BF00540125

    Article  Google Scholar 

  • Kimbrell T, Holt RD, Lundberg P (2007) The influence of vigilance on intraguild predation. J Theor Biol 249:218–234. doi:10.1016/j.jtbi.2007.07.031

    Article  PubMed  Google Scholar 

  • Korpimäki E, Marti CD (1995) Geographical trends in trophic characteristics of mammal-eating and bird-eating raptors in Europe and North America. Auk 112:1004–1023

    Google Scholar 

  • MacArthur RH, Pianka ER (1966) On optimal use of a patchy environment. Am Nat 100:603–609. doi:10.1086/282454

    Article  Google Scholar 

  • MacDonald DW, Barret P (1993) Mammals of Britain and Europe. Harper-Collins, London

    Google Scholar 

  • Mañosa S (1994) Goshawk diet in a Mediterranean area of Northeastern Spain. J Raptor Res 28:84–92

    Google Scholar 

  • Marquiss M, Ratcliffe DA, Roxburgh R (1985) The numbers, breeding success and diet of golden eagles in Southern Scotland in relation to changes in land use. Biol Conserv 34:121–140. doi:10.1016/0006-3207(85)90104-1

    Article  Google Scholar 

  • Martínez JE, Calvo JF (2001) Diet and breeding success of eagle owl in Southeastern Spain: effect of rabbit haemorrhagic disease. J Raptor Res 35:259–262

    Google Scholar 

  • Martínez JA, Zuberogoitia I (2001) The response of the eagle owl (Bubo bubo) to an outbreak of the rabbit haemorrhagic disease. J Ornithol 142:204–211. doi:10.1007/BF01651788

    Article  Google Scholar 

  • Menge BA, Sutherland JP (1976) Species diversity gradients: synthesis of the roles of predation, competition, and temporal heterogeneity. Am Nat 110:351–369. doi:10.1086/283073

    Article  Google Scholar 

  • Mikkola H (1976) Owls killing and killed by other owls and raptors in Europe. Br Birds 69:144–154

    Google Scholar 

  • Moleón M, Almaraz P, Sánchez-Zapata JA (2008) An emerging infectious disease triggering large-scale hyperpredation. Plos One 3:e2307. doi:10.1371/journal.pone.0002307

    Article  PubMed  Google Scholar 

  • Moleón M, Sánchez-Zapata JA, Real J, García-Charton JA, Gil-Sánchez JM, Palma L, Bautista J, Bayle P (2009) Large-scale spatio-temporal shifts in the diet of a predator mediated by an emerging infectious disease of its main prey. J Biogeogr 36:1502–1515. doi:10.1111/j.1365-2699.2009.02078.x

    Article  Google Scholar 

  • Morin P (1999) Productivity, intraguild predation, and population dynamics in experimental food webs. Ecology 80:752–760. doi:10.1890/0012-9658(1999)080[0752:PIPAPD]2.0.CO;2

    Article  Google Scholar 

  • Mylius SD, Klumpers K, de Roos AM, Persson L (2001) Impact of intraguild predations and stage structure on simple communities along a productivity gradient. Am Nat 158:259–276. doi:10.1086/321321

    Article  CAS  PubMed  Google Scholar 

  • Newton I (1979) Population ecology of raptors. Poyser, London

    Google Scholar 

  • Nielsen JT, Drachmann J (1999) Prey selection of Goshawks Accipiter gentilis during the breeding season in Vendsyssel, Denmark. Dansk Orn Foren Tidsskr 93:85–90

    Google Scholar 

  • Nyström J, Ekenstedt J, Angerbjörn A, Thulin L, Hellström P, Dalén L (2006) Golden eagles on the Swedish mountain tundra—diet and breeding success in relation to prey fluctuations. Ornis Fenn 83:145–152

    Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D’Amico JA, Itoua I, Strand HE, Morrison JH, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on earth. Bioscience 51:933–938. doi:10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Article  Google Scholar 

  • Palomares F, Caro TM (1999) Interspecific killing among mammalian carnivores. Am Nat 153:492–508. doi:10.1086/303189

    Article  Google Scholar 

  • Palomares F, Gaona P, Ferreras P, Delibes M (1995) Positive effects on game species of top predators by controlling smaller predator populations: an example with lynx, mongooses, and rabbits. Conserv Biol 9:295–305. doi:10.1046/j.1523-1739.1995.9020295.x

    Article  Google Scholar 

  • Palomares F, Ferreras P, Fedriani JM, Delibes M (1996) Spatial relationships between Iberian lynx and other carnivores in an area of south-western Spain. J Appl Ecol 33:5–13

    Article  Google Scholar 

  • Pedrini P, Sergio F (2001) Density, productivity, diet, and human persecution of golden eagles (Aquila chrysaetos) in the Central-Eastern Italian Alps. J Raptor Res 35:40–48

    Google Scholar 

  • Pedrini P, Sergio F (2002) Regional conservation priorities for a large predator: golden eagles (Aquila chrysaetos) in the Alpine range. Biol Conserv 103:163–172. doi:10.1016/S0006-3207(01)00116-1

    Article  Google Scholar 

  • Pianka ER (1966) Latitudinal gradients in species diversity: a review of concepts. Am Nat 100:33–46. doi:10.1086/282398

    Article  Google Scholar 

  • Pimm SL, Lawton JH (1978) On feeding on more than one trophic level. Nature 275:542–544. doi:10.1038/275542a0

    Article  Google Scholar 

  • Pinheiro JC, Bates DM (2000) Mixed-effects models in S and S-PLUS. Springer, New York

    Book  Google Scholar 

  • Pinheiro JC, Bates D, DebRoy S, Sarkar D, R Core Team (2008) nlme: linear and nonlinear mixed effects models. R package version 3.1-90

  • Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330. doi:10.1146/annurev.es.20.110189.001501

    Article  Google Scholar 

  • R Development Core Team (2009) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org

  • Real J, Mañosa S (1990) Eagle Owl (Bubo bubo) predation on juvenile Bonelli’s eagles (Hieraaetus fasciatus). J Raptor Res 24:69–71

    Google Scholar 

  • Rutz C, Bijlsma RG (2006) Food-limitation in a generalist predator. Proc R SocLond B 273:2069–2076. doi:10.1098/rspb.2006.3507

    Article  Google Scholar 

  • Salo P, Nordström M, Thomson RL, Korpimäki E (2008) Risk induced by a native top predator reduces alien mink movements. J Anim Ecol 77:1092–1098. doi:10.1111/j.1365-2656.2008.01430.x

    Article  PubMed  Google Scholar 

  • Seguin JF, Thibault JC, Torre J, Bayle P, Vigne JD (2001) The diet of young golden eagles Aquila chrysaetos in Corsica: foraging in a man-made mammal fauna. Ardea 89:527–535

    Google Scholar 

  • Sergio F, Hiraldo F (2008) Intraguild predation in raptor assemblages: a review. Ibis 150(S1):132–145. doi:10.1111/j.1474-919X.2008.00786.x

    Article  Google Scholar 

  • Sergio F, Marchesi L, Pedrini P (2003) Spatial refugia and the coexistence of a diurnal raptor with its intraguild owl predator. J Anim Ecol 72:232–245. doi:10.1046/j.1365-2656.2003.00693.x

    Article  Google Scholar 

  • Sergio F, Marchesi L, Pedrini P, Penteriani V (2007) Coexistence of a generalist owl with its intraguild predator: distance-sensitive or habitat-mediated avoidance? Anim Behav 74:1607–1616. doi:10.1016/j.anbehav.2006.10.022

    Article  Google Scholar 

  • Sergio F, Caro T, Brown D, Clucas B, Hunter J, Ketchum J, McHugh K, Hiraldo F (2008) Top predators as conservation tools: ecological rationale, assumptions, and efficacy. Annu Rev Ecol Evol Syst 39:1–19. doi:10.1146/annurev.ecolsys.39.110707.173545

    Article  Google Scholar 

  • Serrano D (2000) Relationship between raptors and rabbits in the diet of eagle owls in southwestern Europe: competition removal or food stress? J Raptor Res 34:305–310

    Google Scholar 

  • Steenhof K, Kochert MN (1988) Dietary responses of three raptor species to changing prey densities in a natural environment. J Anim Ecol 57:37–48

    Article  Google Scholar 

  • Steenhof K, Kochert MN, McDonald TL (1997) Interactive effects of prey and weather on golden eagle reproduction. J Anim Ecol 66:350–362

    Article  Google Scholar 

  • Sunde P, Bølstad MS, Desfor KB (2003) Diurnal exposure as a risk sensitive behaviour in tawny owls Strix aluco? J Avian Biol 34:409–418. doi:10.1111/j.0908-8857.2003.03105.x

    Article  Google Scholar 

  • Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn and Bacon, Boston

    Google Scholar 

  • Tella JL, Mañosa S (1993) Eagle Owl predation on Egyptian vulture and northern goshawk: possible effect of a decrease in European rabbit availability. J Raptor Res 27:111–112

    Google Scholar 

  • Toyne EP (1998) Breeding season diet of the goshawk Accipiter gentilis in Wales. Ibis 140:569–579. doi:10.1111/j.1474-919X.1998.tb04701.x

    Article  Google Scholar 

  • Valkama J, Korpimäki E, Arroyo B, Beja P, Bretagnolle V, Bro E, Kenward R, Mañosa S, Redpath SM, Thirgood S, Viñuela J (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review. Biol Rev 80:171–203. doi:10.1017/S146479310400658X

    Article  PubMed  Google Scholar 

  • Vance-Chalcraft HD, Rosenheim JA, Vonesh JR, Osenberg CW, Sih A (2007) The influence of intraguild predation on prey suppression and prey release: a meta-analysis. Ecology 88:2689–2696. doi:10.1890/06-1869.1

    Article  PubMed  Google Scholar 

  • Zuberogoitia I, Martínez JE, Zabala J, Martínez JA, Azkona A, Castillo I, Hidalgo S (2008a) Social interactions between two owl species sometimes associated with intraguild predation. Ardea 96:109–113

    Google Scholar 

  • Zuberogoitia I, Martínez JE, Martínez JA, Zabala J, Calvo JF, Azkona A, Pagán I (2008b) The Dho-gaza and mist-net with Eurasian eagle-owl (Bubo bubo) lure: effectiveness in capturing thirteen species of European raptors. J Raptor Res 42:48–51. doi:10.3356/JRR-05-31.1

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Google Scholar 

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Acknowledgments

We thank Michela Marchi-Bartolozzi for useful comments and English revision, and Maria del Mar Delgado who helped gathering references and ideas. Roger Jovani, José Antonio Sánchez Zapata and an anonymous referee made helpful suggestions that greatly improved the manuscript. During this work R.L. and S.M.S. were supported by doctoral degree grants from Fundação para a Ciência e a Tecnologia, Portugal (respectively, BD/27434/2006 and BD/21403/2005), and V.P. was granted by the Secretaría General de Universidades, Spanish Ministry of Education (Salvador de Madariaga Program).

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Lourenço, R., Santos, S.M., Rabaça, J.E. et al. Superpredation patterns in four large European raptors. Popul Ecol 53, 175–185 (2011). https://doi.org/10.1007/s10144-010-0199-4

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