Advertisement

Oecologia

, Volume 182, Issue 2, pp 487–498 | Cite as

Guardian or threat: does golden eagle predation risk have cascading effects on forest grouse?

  • Mari S. LylyEmail author
  • Alexandre Villers
  • Elina Koivisto
  • Pekka Helle
  • Tuomo Ollila
  • Erkki Korpimäki
Population ecology – original research

Abstract

Previous studies on intraguild predation have mainly focused on within-class assemblages, even though avian top predators may also influence mammalian mesopredator prey. By using nation-wide long-term data from Finland, northern Europe, we examined the impacts of golden eagles (Aquila chrysaetos) together with red foxes (Vulpes vulpes) and pine martens (Martes martes) on forest-dwelling herbivores, black grouse (Tetrao tetrix) and hazel grouse (Tetrastes bonasia). We hypothesized that eagles may alleviate the overall predation pressure on grouse by imposing intraguild predation risk on mesopredators. The predation impact of eagle was modelled using eagle density estimates and distance to eagle nest. Wildlife triangle counts were used as predation impact proxies of mammalian mesopredators and as measures of response in grouse. Our results show that eagle density correlated negatively with black grouse abundance indices while being positively associated with the proportion of juveniles in both grouse species, irrespective of the abundance of mesopredators. Yet, foxes and martens alone had a negative effect on the abundance indices and the proportion of young in the two grouse species. This suggests that the possible cascading effects of eagles are not mediated by decreased mesopredator numbers, but instead by fear effects. Alternatively, they may be mediated by other species than fox or marten studied here. In conclusion, we found support for the hypothesis that eagles provide protection for juvenile black and hazel grouse, whereas they are a threat for adult grouse. This important information helps us to better understand the role of avian top predators in terrestrial ecosystems.

Keywords

Intraguild predation Mesopredator suppression Top predator Trophic cascade 

Notes

Acknowledgments

We thank all the volunteers who have helped to collect the golden eagle, mesopredator and grouse abundance data. We are grateful to Robert L. Thomson for helpful comments on the language and contents of the manuscript. The study was financially supported by the Jenny and Antti Wihuri Foundation (grants to MSL), and the Academy of Finland (Grant Nos. 123379, 136717 and 250709 to EKor).

Author contribution statement

EKor, PH and TO originally formulated the idea. PH and TO coordinated data collection; MSL, AV, EKoi and EKor developed the methodology; MSL and AV analysed the data. MSL, EKoi and EKor wrote the manuscript; other authors provided editorial advice.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2016_3680_MOESM1_ESM.pdf (2.2 mb)
Supplementary material 1 (PDF 2269 kb)

References

  1. Åberg J, Swenson JE, Angelstam P (2003) The habitat requirements of hazel grouse (Bonasa bonasia) in managed boreal forest and applicability of forest stand descriptions as a tool to identify suitable patches. Forest Ecol Manag 175:437–444. doi: 10.1016/S0378-1127(02)00144-5 CrossRefGoogle Scholar
  2. Angelstam P (2004) Habitat thresholds and effects of forest landscape change on the distribution and abundance of black grouse and capercaillie. Ecol Bull 51:173–187Google Scholar
  3. Baddeley A, Turner R (2005) spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12:1–42CrossRefGoogle Scholar
  4. Banks PB, Nordström M, Ahola M et al (2008) Impacts of alien mink predation on island vertebrate communities of the Baltic Sea archipelago: review of a long-term experimental study. Boreal Environ Res 13:3–16Google Scholar
  5. Bêty J, Gauthier G, Giroux J-F, Korpimäki E (2001) Are goose nesting success and lemming cycles linked? Interplay between nest density and predators. Oikos 93:388–400CrossRefGoogle Scholar
  6. Bjornstad ON (2015) ncf: spatial nonparametric covariance functions. R package version 1.1-6. https://CRAN.R-project.org/package=ncf
  7. Brainerd SM, Rolstad J (2002) Habitat selection by Eurasian pine martens Martes martes in managed forests of southern boreal Scandinavia. Wildlife Biol 8:289–297Google Scholar
  8. Core Team R (2015) R: a language and environment for statistical computing. Version 3(2):3Google Scholar
  9. Crooks KR, Soulé ME (1999) Mesopredator release and avifaunal extinctions in a fragmented system. Nature 400:563–566. doi: 10.1038/23028 CrossRefGoogle Scholar
  10. Dell’Arte GL, Laaksonen T, Norrdahl K, Korpimäki E (2007) Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey. Acta Oecol 31:276–281. doi: 10.1016/j.actao.2006.12.007 CrossRefGoogle Scholar
  11. Elmhagen B, Ludwig G, Rushton SP et al (2010) Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. J Anim Ecol 79:785–794. doi: 10.1111/j.1365-2656.2010.01678.x PubMedGoogle Scholar
  12. Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet Earth. Science 333:301–306. doi: 10.1126/science.1205106 CrossRefPubMedGoogle Scholar
  13. European Environment Agency (2009) CORILIS—CORINE Lissage (2000). European Union Open Data Portal. Permalink: 63eabc5a1a61b356b891c48638c519f3Google Scholar
  14. Fey K, Banks PB, Oksanen L, Korpimäki E (2009) Does removal of an alien predator from small islands in the Baltic Sea induce a trophic cascade? Ecography 32:546–552. doi: 10.1111/j.1600-0587.2008.05637.x CrossRefGoogle Scholar
  15. Finnish Meteorological Institute (2014) Open data: Finnish Climate Data set 1961–2000Google Scholar
  16. Hakkarainen H, Korpimäki E (1996) Competitive and predatory interactions among raptors: an observational and experimental study. Ecology 77:1134–1142CrossRefGoogle Scholar
  17. Hanski I, Henttonen H, Korpimäki E et al (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520CrossRefGoogle Scholar
  18. Kauhala K, Laukkanen P, von Rége I (1998) Summer food composition and food niche overlap of the raccoon dog, red fox and badger in Finland. Ecography 21:457–463. doi: 10.1111/j.1600-0587.1998.tb00436.x CrossRefGoogle Scholar
  19. Kauhala K, Helle P, Helle E (2000) Predator control and the density and reproductive success of grouse populations in Finland. Ecography 23:161–168. doi: 10.1034/j.1600-0587.2000.230201.x CrossRefGoogle Scholar
  20. Korpimäki E, Norrdahl K (1989) Avian predation on mustelids in Europe 1: occurrence and effects on body size variation and life traits. Oikos 55:205–215. doi: 10.2307/3565424 CrossRefGoogle Scholar
  21. Korpimäki E, Norrdahl K, Huitu O, Klemola T (2005) Predator-induced synchrony in population oscillations of coexisting small mammal species. Proc R Soc B Biol Sci 272:193–202. doi: 10.1098/rspb.2004.2860 CrossRefGoogle Scholar
  22. Kurki S, Helle P, Lindén H, Nikula A (1997) Breeding success of black grouse and capercaillie in relation to mammalian predator densities on two spatial scales. Oikos 79:301–310. doi: 10.2307/3546014 CrossRefGoogle Scholar
  23. Kurki S, Nikula A, Helle P, Lindén H (1998) Abundances of red fox and pine marten in relation to the composition of boreal forest landscapes. J Anim Ecol 67:874–886. doi: 10.1046/j.1365-2656.1998.6760874.x CrossRefPubMedGoogle Scholar
  24. Lindén H, Helle E, Helle P, Wikman M (1996) Wildlife triangle scheme in Finland: methods and aims for monitoring wildlife populations. Finn Game Res 49:4–11Google Scholar
  25. Lindström ER, Andrén H, Angelstam P et al (1994) Disease reveals the predator: sarcoptic mange, red fox predation, and prey populations. Ecology 75:1042–1049CrossRefGoogle Scholar
  26. Lindström ER, Brainerd SM, Helldin JO, Overskaug K (1995) Pine marten-red fox interactions: a case of intraguild predation? Ann Zool Fenn 32:123–130Google Scholar
  27. Lourenço R, Penteriani V, Rabaça JE, Korpimäki E (2014) Lethal interactions among vertebrate top predators: a review of concepts, assumptions and terminology. Biol Rev 89:270–283. doi: 10.1111/brv.12054 CrossRefPubMedGoogle Scholar
  28. Lourenҫo R, Santos SM, Rabaҫa JE, Penteriani V (2011) Superpredation patterns in four large European raptors. Popul Ecol 53:175–185. doi: 10.1007/s10144-010-0199-4 CrossRefGoogle Scholar
  29. Ludwig GX, Alatalo RV, Helle P et al (2006) Short- and long-term population dynamical consequences of asymmetric climate change in black grouse. Proc R Soc B 273:2009–2016. doi: 10.1098/rspb.2006.3538 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ludwig GX, Alatalo RV, Helle P, Siitari H (2010) Individual and environmental determinants of daily black grouse nest survival rates at variable predator densities. Ann Zool Fenn 47:387–397CrossRefGoogle Scholar
  31. Lyly MS, Villers A, Koivisto E et al (2015) Avian top predator and the landscape of fear: responses of mammalian mesopredators to risk imposed by the golden eagle. Ecol Evol 5:503–514. doi: 10.1002/ece3.1370 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Marcström V, Kenward RE, Engren E (1988) The impact of predation on boreal tetraonids during vole cycles: an experimental study. J Anim Ecol 57:859–872. doi: 10.2307/5097 CrossRefGoogle Scholar
  33. Marjakangas A, Rintamäki H, Hissa R (1984) Thermal responses in the capercaillie Tetrao urogallus and the black grouse Lyrurus tetrix roosting in the snow. Physiol Zool 57:99–104CrossRefGoogle Scholar
  34. Mönkkönen M, Husby M, Tornberg R et al (2007) Predation as a landscape effect: the trading off by prey species between predation risks and protection benefits. J Anim Ecol 76:619–629. doi: 10.1111/j.1365-2656.2007.01233.x CrossRefPubMedGoogle Scholar
  35. Montadert M, Leonard P (2003) Survival in an expanding hazel grouse Bonasa bonasia population in the southeastern French Alps. Wildlife Biol 9:357–364Google Scholar
  36. Newsome TM, Ripple WJ (2015) A continental scale trophic cascade from wolves through coyotes to foxes. J Anim Ecol 84:49–59. doi: 10.1111/1365-2656.12258 CrossRefPubMedGoogle Scholar
  37. Ollila T (2015) Raportti maakotkan, muuttohaukan, tunturihaukan sekä Oulun ja Lapin läänien merikotkien pesinnöistä vuonna 2015. Luontopalvelut, MetsähallitusGoogle Scholar
  38. Ollila T, Ilmonen J (2009) Metsähallituksen vastuulajien tila ja suojelutaso vuonna 2006. Maakotka—Aquila chrysaetos (L.). Tietolomake, lajit. MetsähallitusGoogle Scholar
  39. 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 9:295–305CrossRefGoogle Scholar
  40. Pekkola M, Alatalo R, Pöysä H, Siitari H (2014) Seasonal survival of young and adult black grouse females in boreal forests. Eur J Wildl Res 60:477–488. doi: 10.1007/s10344-014-0809-0 CrossRefGoogle Scholar
  41. Pellikka J, Rita H, Lindén H (2005) Monitoring wildlife richness—Finnish applications based on wildlife triangle censuses. Ann Zool Fenn 42:123–134Google Scholar
  42. 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 CrossRefGoogle Scholar
  43. Prugh LR, Stoner CJ, Epps CW et al (2009) The rise of the mesopredator. Bioscience 59:779–791. doi: 10.1525/bio.2009.59.9.9 CrossRefGoogle Scholar
  44. Pulliainen E, Ollinmäki P (1996) A long-term study of the winter food niche of the pine marten Martes martes in northern boreal Finland. Acta Theriol 41:337–352CrossRefGoogle Scholar
  45. Quinn JL, Ueta M (2008) Protective nesting associations in birds. Ibis 150:146–167. doi: 10.1111/j.1474-919X.2008.00823.x CrossRefGoogle Scholar
  46. Quinn JL, Prop J, Kokorev Y, Black JM (2003) Predator protection or similar habitat selection in red-breasted goose nesting associations: extremes along a continuum. Anim Behav 65:297–307. doi: 10.1006/anbe.2003.2063 CrossRefGoogle Scholar
  47. Ripple WJ, Beschta RL (2012) Trophic cascades in Yellowstone: the first 15 years after wolf reintroduction. Biol Conserv 145:205–213. doi: 10.1016/j.biocon.2011.11.005 CrossRefGoogle Scholar
  48. Ritchie EG, Elmhagen B, Glen AS et al (2012) Ecosystem restoration with teeth: what role for predators? Trends Ecol Evol 27:265–271. doi: 10.1016/j.tree.2012.01.001 CrossRefPubMedGoogle Scholar
  49. Roemer GW, Gompper ME, van Valkenburgh B (2009) The ecological role of the mammalian mesocarnivore. Bioscience 59:165–173. doi: 10.1525/bio.2009.59.2.9 CrossRefGoogle Scholar
  50. 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 CrossRefPubMedGoogle Scholar
  51. Saniga M (2002) Nest loss and chick mortality in capercaillie (Tetrao urogallus) and hazel grouse (Bonasa bonasia) in West Carpathians. Folia Zool 51:205–214Google Scholar
  52. Sergio F, Hiraldo F (2008) Intraguild predation in raptor assemblages: a review. Ibis 150:132–145. doi: 10.1111/j.1474-919X.2008.00786.x CrossRefGoogle Scholar
  53. Sih A, Englund G, Wooster D (1998) Emergent impacts of multiple predators on prey. Trends Ecol Evol 13:350–355CrossRefPubMedGoogle Scholar
  54. Storch I, Lindström E, de Jounge J (1990) Diet and habitat selection of the pine marten in relation to competition with the red fox. Acta Theriol 35:311–320CrossRefGoogle Scholar
  55. Sulkava S, Huhtala K, Rajala P, Tornberg R (1999) Changes in the diet of the Golden Eagle Aquila chrysaetos and small game populations in Finland in 1957–96. Ornis Fenn 76:1–16Google Scholar
  56. Swenson JE, Angelstam P (1993) Habitat separation by sympatric forest grouse in Fennoscandia in relation to boreal forest succession. Can J Zool 71:1303–1310. doi: 10.1139/z93-180 CrossRefGoogle Scholar
  57. Swenson JE, Saari L, Bonczar Z (1994) Effects of weather on hazel grouse reproduction: an allometric perspective. J Avian Biol 25:8–14CrossRefGoogle Scholar
  58. Terborgh J, Estes JA (2010) Trophic cascades: predators, prey and the changing dynamics of nature. Island Press, Washington DCGoogle Scholar
  59. Tornberg R (2001) Pattern of goshawk Accipiter gentilis predation on four forest grouse species in northern Finland. Wildlife Biol 7:245–256Google Scholar
  60. Tornberg R, Helle P, Korpimäki E (2011) Vulnerability of black grouse hens to goshawk predation: result of food supply or predation facilitation? Oecologia 166:577–584. doi: 10.1007/s00442-010-1884-x CrossRefPubMedGoogle Scholar
  61. Valkama J, Korpimäki E, Arroyo B et al (2005) Birds of prey as limiting factors of gamebird populations in Europe: a review. Biol Rev 80:171–203. doi: 10.1017/s146479310400658x CrossRefPubMedGoogle Scholar
  62. Vance-Chalcraft HD, Rosenheim JA, Vonesh JR et al (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 CrossRefPubMedGoogle Scholar
  63. Watson J (2010) The Golden Eagle, 2nd edn. Yale University Press, New HavenGoogle Scholar
  64. Wood S (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc 73:3–36CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Mari S. Lyly
    • 1
    Email author
  • Alexandre Villers
    • 1
    • 2
  • Elina Koivisto
    • 1
  • Pekka Helle
    • 3
  • Tuomo Ollila
    • 4
  • Erkki Korpimäki
    • 1
  1. 1.Section of Ecology, Department of BiologyUniversity of TurkuTurkuFinland
  2. 2.Centre d’Etudes Biologiques de Chizé UMR 7372CNRS and Université de La RochelleVilliers-en-BoisFrance
  3. 3.Natural Resources Institute Finland, Oulu Game and Fisheries ResearchUniversity of OuluOuluFinland
  4. 4.Metsähallitus, Parks and WildlifeRovaniemiFinland

Personalised recommendations