Skip to main content
Log in

Functional responses of the rough-legged buzzard in a multi-prey system

  • Population ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The functional response is a key element of predator–prey interactions. Basic functional response theory explains foraging behavior of individual predators, but many empirical studies of free-ranging predators have estimated functional responses by using population-averaged data. We used a novel approach to investigate functional responses of an avian predator (the rough legged-buzzard Buteo lagopus Pontoppidan, 1763) to intra-annual spatial variation in rodent density in subarctic Sweden, using breeding pairs as the sampling unit. The rough-legged buzzards responded functionally to Norwegian lemmings (Lemmus lemmus L. 1758), grey-sided voles (Myodes rufocanus Sundevall, 1846) and field voles (Microtus agrestis L. 1761), but different rodent prey were not utilised according to relative abundance. The functional response to Norwegian lemmings was a steep type II curve and a more shallow type III response to grey-sided voles. The different shapes of these two functional responses were likely due to combined effects of differences between lemmings and grey-sided voles in habitat utilisation, anti-predator behaviour and size-dependent vulnerability to predation. Diet composition changed less than changes in relative prey abundance, indicating negative switching, with high disproportional use of especially lemmings at low relative densities. Our results suggest that lemmings and voles should be treated separately in future empirical and theoretical studies in order to better understand the role of predation in this study system.

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

  • Abrams P (1987) The functional responses of adaptive consumers of two resources. Theor Popul Biol 32:262–288. doi:10.1016/0040-5809(87)90050-5

    Google Scholar 

  • Abrams PA (1994) The fallacies of ‘ratio-dependent’ predation. Ecology 75:1842–1850. doi:10.2307/1939644

    Google Scholar 

  • Abrams PA, Ginzburg LR (2000) The nature of predation: prey dependent, ratio dependent or neither? Trends Ecol Evol 15:337–341. doi:10.1016/S0169-5347(00)01908-X

    PubMed  Google Scholar 

  • Abrams P, Matsuda H (1993) Effects of adaptive predatory and anti-predator behaviour in a two-prey-one-predator system. Evol Ecol 7:312–326. doi:10.1007/BF01237749

    Google Scholar 

  • Andersson M (1976) Lemmus lemmus: a possible case of aposematic coloration and behavior. J Mammal 57:461–469. doi:10.2307/1379296

    Google Scholar 

  • Arditi R, Ginzburg LR (1989) Coupling in predator-prey dynamics: ratio-dependence. J Theor Biol 139:311–326. doi:10.1016/S0022-5193(89)80211-5

    Google Scholar 

  • Asseburg C (2006) A Bayesian approach to modelling field data on multi-species predator-prey interactions. PhD thesis, University of St. Andrews, St. Andrews

  • Barth L, Angerbjörn A, Tannerfeldt M (2000) Are Norwegian lemmings Lemmus lemmus avoided by arctic Alopex lagopus or red foxes Vulpes vulpes? A feeding experiment. Wildl Biol 6:101–109

    Google Scholar 

  • Boutin S (1995) Testing predator-prey theory by studying fluctuating populations of small mammals. Wildl Res 22:89–100. doi:10.1071/WR9950089

    Google Scholar 

  • Brom TG (1986) Microscopic identification of feathers and feather fragments of palearctic birds. Bijdr Dierkunde 56:181–204

    Google Scholar 

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

  • Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519. doi:10.1016/j.ecolmodel.2006.03.017

    Google Scholar 

  • Chesson J (1978) Measuring preference in selective predation. Ecology 59:211–215. doi:10.2307/1936364

    Google Scholar 

  • Chesson PL (1984) Variable predators and switching behavior. Theor Popul Biol 26:1–26. doi:10.1016/0040-5809(84)90021-2

    Google Scholar 

  • Cornulier T, Yoccoz NG, Bretagnolle V, Brommer JE, Butet A, Ecke F, Elston DA, Framstad E, Henttonen H, Hörnfeldt B, Huitu O, Imholt C, Ims RA, Jacob J, Jedrzejewska B, Millon A, Petty S, Pietiäinen H, Tkadlec E, Zub K, Lambin X (2013) Europe-wide dampening of population cycles in keystone herbivores. Science 340:63–66. doi:10.1126/science.1228992

    CAS  PubMed  Google Scholar 

  • Cramp S, Simmons KEL (eds) (1980) The birds of the Western Palearctic, vol 2. Oxford University Press, Oxford

    Google Scholar 

  • Davoren GK, Burger AE (1999) Differences in prey selection and behaviour during self-feeding and chick provisioning in rhinoceros auklets. Anim Behav 58:853–863. doi:10.1006/anbe.1999.1209

    PubMed  Google Scholar 

  • Day MG (1966) Identification of hair and feather remains in the gut and faeces of stoats and weasels. J Zool 148:201–217. doi:10.1111/j.1469-7998.1966.tb02948.x

    Google Scholar 

  • Development Core Team R (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dickman CR (1992) Predation and habitat shift in the house mouse, Mus domesticus. Ecology 73:313–322. doi:10.2307/1938742

    Google Scholar 

  • Dickman CR, Predavec M, Lynam AJ (1991) Differential predation of size and sex classes of mice by the barn owl, Tyto alba. Oikos 62:67–76. doi:10.2307/3545447

    Google Scholar 

  • Ecke F, Christensen P, Rentz R, Nilsson M, Sandström P, Hörnfeldt B (2010) Landscape structure and the long-term decline of cyclic grey-sided voles in Fennoscandia. Landsc Ecol 25:551–560. doi:10.1007/s10980-009-9441-x

    Google Scholar 

  • Ekerholm P, Oksanen L, Oksanen T (2001) Long-term dynamics of voles and lemmings at the timberline and above the willow limit as a test of hypotheses on trophic interactions. Ecography 24:555–568. doi:10.1034/j.1600-0587.2001.d01-211.x

    Google Scholar 

  • Englund G, Leonardsson K (2008) Scaling up the functional response for spatially heterogeneous systems. Ecol Lett 11:440–449. doi:10.1111/j.1461-0248.2008.01159.x

    PubMed  Google Scholar 

  • Falck W, Bjørnstad ON, Stenseth NC (1995) Voles and lemmings: chaos and uncertainty in fluctuating populations. Proc R Soc Lond B 262:363–370. doi:10.1098/rspb.1995.0218

    Google Scholar 

  • Framstad E, Stenseth NC, Bjørnstad ON, Falck W (1997) Limit cycles in Norwegian lemmings: tensions between phase-dependence and density-dependence. Proc R Soc Lond B 264:31–38. doi:10.1098/rspb.1997.0005

    Google Scholar 

  • Fryxell JM, Lundberg P (1998) Individual behaviour and community dynamics. Chapman & Hall, London

    Google Scholar 

  • Gruyer N, Gauthier G, Berteaux D (2008) Cyclic dynamics of sympatric lemming populations on Bylot Island, Nunavut, Canada. Can J Zool 86:910–917. doi:10.1139/Z08-059

    Google Scholar 

  • Hagemeijer WJM, Blair MJ (1997) The EBCC atlas of European breeding birds. Poyser, London

    Google Scholar 

  • Hagen Y (1952) Rovfuglene og viltpleien. Gyldendal Norsk, Oslo

    Google Scholar 

  • Hagen Y (1969) Norske undersøkelser over avkomproduksjonen hos rovfugler og ugler sett i relasjon til smågnagerbestandens vekslinger. Fauna 22:73–126

    Google Scholar 

  • Hakkarainen H, Korpimäki E, Mappes T, Palokangas P (1992) Kestrel hunting behaviour towards solitary and grouped Microtus agrestis and M. epiroticus—a laboratory experiment. Ann Zool Fenn 29:279–284

    Google Scholar 

  • Hambäck PA, Schneider M, Oksanen T (1998) Winter herbivory by voles during a population peak: the relative importance of local factors and landscape pattern. J Anim Ecol 67:544–553. doi:10.1046/j.1365-2656.1998.00231.x

    Google Scholar 

  • Hansen TF, Stenseth NC, Henttonen H (1999) Multiannual vole cycles and population regulation during long winters: an analysis of seasonal density dependence. Am Nat 154:129–139. doi:10.1086/303229

    Google Scholar 

  • Hanski I, Henttonen H (1996) Predation on competing rodent species: a simple explanation of complex patterns. J Anim Ecol 65:220–232. doi:10.2307/5725

    Google Scholar 

  • Hanski I, Henttonen H, Hansson L (1994) Temporal variability and geographical patterns in the population density of microtine rodents: a reply to Xia and Boonstra. Am Nat 144:329–342. doi:10.1086/285678

    Google Scholar 

  • Hanski I, Henttonen H, Korpimäki E, Oksanen L, Turchin P (2001) Small-rodent dynamics and predation. Ecology 82:1505–1520. doi:10.2307/2679796

    Google Scholar 

  • Hellström P (2007) Interactions between rodents and rough-legged buzzards (Buteo lagopus) in northern Sweden. Phil. lic. thesis, Stockholm University, Stockholm

  • Henttonen H, Hanski I (2000) Population dynamics of small rodents in northern Fennoscandia. In: Perry JN, Smith RH, Woiwood IP (eds) Chaos in Real Data. Kluwer, Dordrecht, pp 73–96

    Google Scholar 

  • Henttonen H, Kaikusalo A (1993) Lemming movements. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic Press, London, pp 157–186

    Google Scholar 

  • Henttonen H, Wallgren H (2001) Rodent dynamics and communities in the birch forest zone of northern Fennoscandia. In: Wielgolaski FE (ed) Nordic Mountain Birch Ecosystems. UNESCO, Carnforth

    Google Scholar 

  • Henttonen H, Oksanen T, Jortikka A, Haukisalmi V (1987) How much do weasels shape microtine cycles in the northern Fennoscandian taiga? Oikos 50:353–365. doi:10.2307/3565496

    Google Scholar 

  • Heske EJ, Steen H (1993) Interspecific interactions and microhabitat use in a Norwegian low alpine rodent assemblage. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 397–409

    Google Scholar 

  • Holling CS (1959a) The components of predation as revealed by a study of small mammal predation of the European pine sawfly. Can Entomol 91:293–320

    Google Scholar 

  • Holling CS (1959b) Some characteristics of simple types of predation and parasitism. Can Entomol 91:385–398

    Google Scholar 

  • Huhtala K, Pulliainen E, Jussila P, Tunkkari PS (1996) Food niche of the gyrfalcon Falco rusticolus nesting in the far north of Finland compared with other choices of the species. Ornis Fenn 73:78–87

    Google Scholar 

  • Ims RA, Fuglei E (2005) Trophic interaction cycles in tundra ecosystems and the impact of climate change. Bioscience 55:311–322. doi:10.1641/0006-3568(2005)055[0311:TICITE]2.0.CO;2

    Google Scholar 

  • Ims RA, Yoccoz NG, Killengreen ST (2011) Determinants of lemming outbreaks. Proc Natl Acad Sci USA 108:1970–1974. doi:10.1073/pnas.1012714108

    CAS  PubMed Central  PubMed  Google Scholar 

  • Inchausti P, Ballesteros S (2008) Intuition, functional responses and the formulation of predator–prey models when there is a large disparity in the spatial domains of the interacting species. J Anim Ecol 77:891–897. doi:10.1111/j.1365-2656.2008.01419.x

    CAS  PubMed  Google Scholar 

  • Johannesen E, Mauritzen M (1999) Habitat selection of grey-sided voles and bank voles in two subalpine populations in southern Norway. Ann Zool Fenn 36:215–222

    Google Scholar 

  • Jost C, Devulder G, Vucetich JA, Peterson RO, Arditi R (2005) The wolves of Isle Royale display scale-invariant satiation and ratio-dependent predation on moose. J Anim Ecol 74:809–816. doi:10.1111/j.1365-2656.2005.00977.x

    Google Scholar 

  • Kean-Howie JC, Pearre S Jr, Dickie LM (1988) Experimental predation by sticklebacks on larval mackerel and protection of fish larvae by zooplankton alternative prey. J Exp Mar Biol Ecol 124:239–259. doi:10.1016/0022-0981(88)90174-8

    Google Scholar 

  • Koen-Alonso M (2007) A process-oriented approach to the multispecies functional response. In: Rooney N, McCann KS, Noakes DLG (eds) From energetics to ecosystems: the dynamics and structure of ecological systems. Springer, Dordrecht

    Google Scholar 

  • Koivunen V, Korpimäki E, Hakkarainen H, Norrdahl K (1996) Prey choice of Tengmalm’s owls (Aegolius funereus): preference for substandard individuals? Can J Zool 74:816–823. doi:10.1139/z96-094

    Google Scholar 

  • Koponen T, Kokkonen A, Kalela O (1961) On a case of spring migration in the Norwegian lemming. Ann Acad Sci Fenn Ser A 52:1–30

    Google Scholar 

  • Korpimäki E, Tolonen P, Valkama J (1994) Functional responses and load-size effect in central place foragers: data from the kestrel and some general comments. Oikos 69:504–510. doi:10.2307/3545862

    Google Scholar 

  • Korpimäki E, Norrdahl K, Klemola T, Pettersen T, Stenseth NC (2002) Dynamic effects of predators on cyclic voles: field experimentation and model extrapolation. Proc R Soc Lond B 269:991–997. doi:10.1098/rspb.2002.1972

    Google Scholar 

  • Krebs CJ, Myers JH (1974) Population cycles in small mammals. Adv Ecol Res 8:267–399. doi:10.1016/S0065-2504(08)60280-9

    Google Scholar 

  • Krebs CJ, Kenney AJ, Gilbert S, Danell K, Angerbjörn A, Erlinge S, Bromley RG, Shank C, Carriere S (2002) Synchrony in lemming and vole populations in the Canadian arctic. Can J Zool 80:1323–1333. doi:10.1139/z02-120

    Google Scholar 

  • Kuno E (1987) Principles of predator-prey interaction in theoretical, experimental, and natural population systems. Adv Ecol Res 16:249–337. doi:10.1016/S0065-2504(08)60090-2

    Google Scholar 

  • Lindén H, Wikman M (1983) Goshawk predation on tetraonids: availability of prey and diet of the predator in the breeding season. J Anim Ecol 52:953–968. doi:10.2307/4466

    Google Scholar 

  • Magnusson M, Bergsten A, Ecke F, Bodin Ö, Bodin L, Hörnfeldt B (2013) Predicting grey-sided vole occurrence in northern Sweden at multiple spatial scales. Ecol Evol 3:4365–4376. doi:10.1002/ece3.827

    PubMed Central  PubMed  Google Scholar 

  • Manly BFJ, Miller P, Cook LM (1972) Analysis of a selective predation experiment. Am Nat 106:719–736. doi:10.1086/282808

    Google Scholar 

  • Manly BFJ, McDonald LL, Thomas DL, McDonald TL, Erickson WP (2002) Resource selection by animals—statistical design and analysis for field studies, 2nd edn. Kluwer, Dordrecht

    Google Scholar 

  • Markman S, Pinshow B, Wright J, Kotler BP (2004) Food patch use by parent birds: to gather food for themselves or for their chicks? J Anim Ecol 73:747–755. doi:10.1111/j.0021-8790.2004.00847.x

    Google Scholar 

  • Matthiopoulos J, Graham K, Smout S, Asseburg C, Redpath S, Thirgood S, Hudson P, Harwood J (2007) Sensitivity to assumptions in models of generalist predation on a cyclic prey. Ecology 88:2576–2586. doi:10.1890/06-0483.1

    PubMed  Google Scholar 

  • Messier F (1995) On the functional and numerical responses of wolves to changing prey density. In: Carbyn LN, Fritts SH, Seip DR (eds) Ecology and conservation of wolves in a changing world. Canadian Circumpolar Institute, Edmonton, pp 187–197

    Google Scholar 

  • Moleón M, Sánchez-Zapata JA, Gil-Sánchez JM, Ballesteros-Duperón E, Barea-Azcón JM, Virgós E (2012) Predator–prey relationships in a Mediterranean vertebrate system: Bonelli’s eagles, rabbits and partridges. Oecologia (Berl) 168:679–689. doi:10.1007/s00442-011-2134-6

    Google Scholar 

  • Murdoch WW (1969) Switching in general predators: experiments on predator specificity and stability of prey populations. Ecol Monogr 39:335–354. doi:10.2307/1942352

    Google Scholar 

  • Murdoch WW, Oaten A (1975) Predation and population stability. Adv Ecol Res 9:1–131. doi:10.1016/S0065-2504(08)60288-3

    Google Scholar 

  • Murdoch WW, Briggs CJ, Nisbet RM (2003) Consumer-resource dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Myllymäki A, Aho J, Lind EA, Tast J (1962) Behaviour and daily activity of the Norwegian lemming, Lemmus lemmus (L.) during autumn migration. Ann Zool Soc Zool Bot Fenn Vanamo 24:1–31

    Google Scholar 

  • Nelson L Jr, Clark FW (1973) Correction for sprung traps in catch/effort calculations of trapping results. J Mammal 54:295–298. doi:10.2307/1378903

    Google Scholar 

  • Niethammer J, Krapp F (eds) (1982) Handbuch der Säugetiere Europas. Band 2/I, Nagetiere II (Cricetidae, Arvicolidae, Zapodidae, Spalacidae, Hystricidae, Capromyidae). Academische, Wiesbaden

  • Nishimura K, Abe MT (1988) Prey susceptibilities, prey utilization and variable attack efficiences of ural owls. Oecologia (Berl) 77:414–422. doi:10.1007/BF00378053

    Google Scholar 

  • Norrdahl K, Korpimäki E (1993) Predation and interspecific competition in two Microtus voles. Oikos 67:149–158. doi:10.2307/3545105

    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 

  • Oaten A, Murdoch WW (1975) Switching, functional response, and stability in predator-prey systems. Am Nat 109:299–318. doi:10.1086/282999

    Google Scholar 

  • O’Donoghue M, Boutin S, Krebs CJ, Murray DL, Hofer EJ (1998) Behavioural responses of coyotes and lynx to the snowshoe hare cycle. Oikos 82:169–183. doi:10.2307/3546927

    Google Scholar 

  • Oksanen T (1993) Does predation prevent Norwegian lemmings from establishing permanent populations in lowland forests? In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 425–437

    Google Scholar 

  • Oksanen T, Henttonen H (1996) Dynamics of voles and small mustelids in the taiga landscape of northern Fennoscandia in relation to habitat quality. Ecography 19:432–443. doi:10.1111/j.1600-0587.1996.tb00254.x

    Google Scholar 

  • Oksanen L, Moen J, Lundberg PA (1992) The time-scale problem in exploiter-victim models: does the solution lie in ratio-dependent exploitation? Am Nat 140:938–960. doi:10.1086/285449

    Google Scholar 

  • Oksanen T, Schneider M, Rammul Ü, Hambäck P, Aunapuu M (1999) Population fluctuations of voles in north Fennocandian tundra: contrasting dynamics in adjacent areas with different habitat composition. Oikos 86:463–478. doi:10.2307/3546651

    Google Scholar 

  • Oksanen T, Oksanen L, Schneider M, Aunapuu M (2001) Regulation, cycles and stability in northern carnivore-herbivore systems: back to first principles. Oikos 94:101–117. doi:10.1034/j.1600-0706.2001.11315.x

    Google Scholar 

  • Oksanen T, Oksanen L, Dahlgren J, Olofsson J (2008) Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol Ecol 10:415–434

    Google Scholar 

  • Olofsson J, Oksanen L, Callaghan T, Hulme PE, Oksanen T, Suominen O (2009) Herbivores inhibit climate-driven shrub expansion on the tundra. Glob Change Biol 15:2681–2693. doi:10.1111/j.1365-2486.2009.01935.x

    Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 155–177

    Google Scholar 

  • Øvrejorde A (2007) Calibrating abundance indices of small rodents in subarctic tundra. MSc thesis, University of Tromsø, Tromsø

  • Palma L, Beja P, Pais M, Cancela da Fonseca L (2006) Why do raptors take domestic prey? The case of Bonelli’s eagles and pigeons. J Appl Ecol 43:1075–1086. doi:10.1111/j.1365-2664.2006.01213.x

    Google Scholar 

  • Pasanen S, Sulkava S (1971) On the nutritional biology of the rough-legged buzzard, Buteo lagopus Brünn., in Finnish Lapland. Aquilo Ser Zool 12:53–63

    Google Scholar 

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

    Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D, The R Development Core Team (2013) nlme: Linear and monlinear mixed effects models. R package version 3.1-113

  • Potapov ER (1993) Ecology and energetics of rough-legged buzzard in the Kolyma river Lowlands. PhD thesis, University of Oxford, Oxford

  • Potapov ER (1997) What determines the population density and reproductive success of rough-legged buzzards, Buteo lagopus, in the Siberian tundra? Oikos 78:362–376

    Google Scholar 

  • Real LA (1977) The kinetics of functional response. Am Nat 111:289–300. doi:10.1086/283161

    Google Scholar 

  • Reid DG, Krebs CJ, Kenney AJ (1997) Patterns of predation on noncyclic lemmings. Ecol Monogr 67:89–108. doi:10.2307/2963506

    Google Scholar 

  • Rindorf A, Gislason H, Lewy P (2006) Prey switching of cod and whiting in the North Sea. Mar Ecol Prog Ser 325:243–253. doi:10.3354/meps325243

    Google Scholar 

  • Rohner C, Krebs CJ (1996) Owl predation on snowshoe hares: consequences of antipredator behaviour. Oecologia (Berl) 108:303–310. doi:10.1007/BF00334655

    Google Scholar 

  • Shifferman E, Eilam D (2004) Movement and direction of movement of a simulated prey affect the success rate in barn owl Tyto alba attack. J Avian Biol 35:111–116. doi:10.1111/j.0908-8857.2004.03257.x

    Google Scholar 

  • Siivonen L (1976) Nordeuropas däggdjur, 2nd edn. Norstedt, Stockholm

    Google Scholar 

  • Sinclair ARE, Pech RP (1996) Density dependence, stochasticity, compensation and predator regulation. Oikos 75:164–173. doi:10.2307/3546240

    Google Scholar 

  • Sinclair ARE, Pech RP, Dickman CR, Hik D, Mahon P, Newsome AE (1998) Predicting effects of predation on conservation of endangered prey. Conserv Biol 12:564–575. doi:10.1046/j.1523-1739.1998.97030.x

    Google Scholar 

  • Solomon ME (1949) The natural control of animal populations. J Anim Ecol 18:1–35. doi:10.2307/1578

    Google Scholar 

  • Sonerud GA (1986) Effect of snow cover on seasonal changes in diet, habitat, and regional distribution of raptors that prey on small mammals in boreal zones of Fennoscandia. Holarct Ecol 9:33–47. doi:10.1111/j.1600-0587.1986.tb01189.x

    Google Scholar 

  • Sonerud GA (1992) Functional responses of birds of prey: biases due to the load-size effect in central place foragers. Oikos 63:223–232. doi:10.2307/3545382

    Google Scholar 

  • Stenseth NC, Ims RA (1993) The biology of lemmings. Academic, London

    Google Scholar 

  • Stephens DW, Krebs CJ (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Sundell J, Ylönen H (2008) Specialist predator in a multi-species prey community: boreal voles and weasels. Integr Zool 3:51–63. doi:10.1111/j.1749-4877.2008.00077.x

    PubMed  Google Scholar 

  • Sundell J, Huitu O, Henttonen H, Kaikusalo A, Korpimäki E, Pietiäinen H, Saurola P, Hanski I (2004) Large-scale spatial dynamics of vole populations in Finland revealed by the breeding success of vole-eating avian predators. J Anim Ecol 73:167–178. doi:10.1111/j.1365-2656.2004.00795.x

    Google Scholar 

  • Sylvén M (1978) Interspecific relations between sympatrically wintering common buzzards Buteo buteo and rough-legged buzzards Buteo lagopus. Ornis Scand 9:197–206. doi:10.2307/3675882

    Google Scholar 

  • Taitt MJ (1993) Adaptive coloration in Lemmus lemmus: why aren’t Norwegian lemmings brown? In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 439–445

    Google Scholar 

  • Taylor A (2009) Grey-sided vole dynamics in mountainous northern Sweden. MSc thesis, Stockholm University, Stockholm

  • Temple SA (1987) Do predators always capture substandard individuals disproportionately from prey populations? Ecology 68:669–674. doi:10.2307/1938472

    Google Scholar 

  • Turchin P (2003) Complex population dynamics. Princeton University Press, Princeton

    Google Scholar 

  • Turchin P, Hanski I (1997) An empirically based model for latitudinal gradient in vole population dynamics. Am Nat 149:842–874. doi:10.1086/286027

    CAS  PubMed  Google Scholar 

  • Turchin P, Oksanen L, Ekerholm P, Oksanen T, Henttonen H (2000) Are lemmings prey or predators? Nature 405:562–565. doi:10.1038/35014595

    CAS  PubMed  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York

    Google Scholar 

  • Wallin L (1967) The dorsal skin gland of the Norwegian lemming Lemmus l. lemmus (L.). Z Morph Ökol Tiere 59:83–90. doi:10.1007/BF02427737

    Google Scholar 

  • White GC, Anderson DR, Burnham KP, Otis DL (1982) Capture-recapture and removal methods for sampling closed populations. Los Alamos National Laboratory, Los Alamos

    Google Scholar 

  • Wiklund CG, Kjellén N, Isakson E (1998) Mechanisms determining the spatial distribution of microtine predators on the Arctic tundra. J Anim Ecol 67:91–98. doi:10.1046/j.1365-2656.1998.00177.x

    Google Scholar 

  • Ydenberg R (2007) Provisioning. In: Stephens DW, Brown JS, Ydenberg RC (eds) Foraging. Behavior and ecology. University of Chicago Press, Chicago, pp 273–303

    Google Scholar 

Download references

Acknowledgments

We are grateful to Johan S. Eklöf for field work, and to Peter Lindberg who conducted surveys in our study area during 1966–1978. Charles J. Krebs gave instructive comments on rodent trapping methods. Geir A. Sonerud, Peter Abrams, Bertil Borg, Love Dalén, Hannu Ylönen, Janne Sundell and anonymous referees provided constructive comments that improved the manuscript. Vattenfall AB, Porjus, supported us with lodging facilities. This project was financed by grants to A. Angerbjörn from The Strategic Foundation for Environmental Research (to the Mountain-MISTRA project), Formas, and Swedish Polar Research Secreteriat/Swedish Research Council. P. Hellström received financial support from Alvin’s foundation for bird protection, the CLUB 300 foundation for bird protection and the Göran Gustafsson foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Hellström.

Additional information

Communicated by Janne Sundell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hellström, P., Nyström, J. & Angerbjörn, A. Functional responses of the rough-legged buzzard in a multi-prey system. Oecologia 174, 1241–1254 (2014). https://doi.org/10.1007/s00442-013-2866-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-013-2866-6

Keywords

Navigation