Abstract
Irruptive migration is mostly observed in species specialized on pulsed resources and is thought to be a response to unpredictable changes in food supply. We assessed two alternative hypotheses to explain the periodic winter irruptions of snowy owls Bubo scandiacus every 3–5 years in temperate North America: (a) the lack-of-food hypothesis, which states that a crash in small mammal abundance on the Arctic breeding grounds forces owls to move out of the tundra massively to search for food in winter; (b) the breeding-success hypothesis, which states that high abundance of tundra small mammals during the summer allows for high production of young, thus increasing the pool of migrants moving south the following winter. We modeled winter irruptions of snowy owls in relation to summer food resources and geographic location. Winter abundance of owls was obtained from citizen-based surveys from 1994 to 2011 and summer abundance of small mammals was collected in summer at two distant sites in Canada: Bylot Island, NU (eastern High Arctic) and Daring Lake, NWT (central Low Arctic). Winter owl abundance was positively related to prey abundance during the previous summer at both sites and tended to decrease from western to eastern temperate North America. Irruptive migration of snowy owls was therefore best explained by the breeding success hypothesis and was apparently caused by large-scale summer variations in food. Our results, combined with previous findings, suggest that the main determinants of irruptive migration may be species specific even in a guild of apparently similar species.
Similar content being viewed by others
References
Angerbjörn A, Tannerfeldt M, Lundberg H (2001) Geographical and temporal patterns of lemming population dynamics in Fennoscandia. Ecography 24:298–308. doi:10.1034/j.1600-0587.2001.240307.x
Bock CE, Lepthien LW (1976) Synchronous eruptions of boreal seed-eating birds. Am Nat 110:559–571. doi:10.1086/283091
Boxall PC, Lein MR (1982) Territoriality and habitat selection of female snowy owls (Nyctea scandiaca) in winter. Can J Zool 60:2344–2350. doi:10.1139/z82-302
Bull EL, Duncan JR (1993) Great gray owl (Strix nebulosa). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca
Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Butcher GS (1990) Audubon Christmas bird counts. In: Sauer JS, Droege S (eds) Survey designs and statistical methods for the estimation of avian population trends. Biological Report, US Fish and Wildlife Service, pp 1–5
Chamberlin ML (1980) Winter hunting behavior of a snowy owl in Michigan. Wilson Bull 92:116–120
Cheveau M, Drapeau P, Imbeau L, Bergeron Y (2004) Owl winter irruptions as an indicator of small mammal population cycles in the boreal forest of eastern North America. Oikos 107:190–198. doi:10.1111/j.0030-1299.2004.13285.x
Chitty H (1950) Canadian arctic wildlife enquiry, 1943–49: with a summary of results since 1933. J Anim Ecol 19:180–193. doi:10.2307/1527
Confer JL, Kanda LL, Li I (2014) Northern saw-whet owl: regional patterns for fall migration and demographics revealed by banding data. Wilson J Ornithol 126:305–320
Côté M, Ibarzabal J, St-Laurent MH, Ferron J, Gagnon R (2007) Age-dependent response of migrant and resident Aegolius owl species to small rodent population fluctuations in the eastern Canadian boreal forest. J Raptor Res 41:16–25. doi:10.3356/0892-1016(2007)41[16:aromar]2.0.co;2
DeLuca W, Holberton R, Hunt PD, Eliason BC (2013) Blackpoll warbler (Setophaga striata). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca
Detienne JC, Holt D, Seidensticker MT, Pitz T (2008) Diet of snowy owls wintering in west-central Montana, with comparisons to other North American studies. J Raptor Res 42:172–179. doi:10.3356/jrr-07-41.1
Dingle H (1972) Migration strategies of insects. Science 175:1327. doi:10.1126/science.175.4028.1327
Dormann CF, McPherson JM, Araujo MB, Bivand R, Bolliger J, Carl G, Davies RG, Hirzel A, Jetz W, Kissling WD, Kuhn I, Ohlemuller R, Peres-Neto PR, Reineking B, Schroder B, Schurr FM, 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
Dunn EH, Francis CM, Blancher PJ, Drennan SR, Howe MA, Lepage D, Robbins CS, Rosenberg KV, Sauer JR, Smith AG (2005) Enhancing the scientific value of the Christmas Bird Count. Auk 122:338–346. doi:10.1642/0004-8038(2005)122[0338:etsvot]2.0.co;2
Elton CS (1924) Periodic fluctuations in the numbers of animals: their causes and effects. Br J Exp Biol 2:119–163
Erlinge S, Danell K, Frodin P, Hasselquist D, Nilsson P, Olofsson EB, Svensson M (1999) Asynchronous population dynamics of Siberian lemmings across the Palaearctic tundra. Oecologia 119:493–500. doi:10.1007/s004420050812
Fauteux D, Cheveau M, Imbeau L, Drapeau P (2015a) Cyclic dynamics of a boreal southern red-backed vole population in northwestern Quebec. J Mammal 96:573–578. doi:10.1093/jmammal/gyv062
Fauteux D, Gauthier G, Berteaux D (2015b) Seasonal demography of a cyclic lemming population in the Canadian Arctic. J Anim Ecol 84:1412–1422. doi:10.1111/1365-2656.12385
Fuller M, Holt D, Schueck L (2003) Snowy owl movements: variation on the migration theme. Springer, Berlin
Gauthier G, Bêty J, Giroux JF, Rochefort L (2004) Trophic interactions in a High Arctic snow goose colony. Integr Comp Biol 44:119–129
Gauthier G, Bêty J, Cadieux MC, Legagneux P, Doiron M, Chevallier C, Lai S, Tarroux A, Berteaux D (2013) Long-term monitoring at multiple trophic levels suggests heterogeneity in responses to climate change in the Canadian Arctic tundra. Philos Trans R Soc B Biol Sci. doi:10.1098/rstb.2012.0482
Gessaman JA (1972) Bioenergetics of the snowy owl (Nyctea scandiaca). Arct Alp Res 4:223–238
Gilchrist HG, Robertson GJ (2000) Observations of marine birds and mammals wintering at polynyas and ice edges in the Belcher Islands, Nunavut, Canada. Arctic 53:61–68
Gilg O, Sittler B, Sabard B, Hurstel A, Sane R, Delattre P, Hanski L (2006) Functional and numerical responses of four lemming predators in High Arctic Greenland. Oikos 113:193–216. doi:10.1111/j.2006.0030-1299.14125.x
Government of the Northwest Territories (2008) Small mammal trapping (museum special traps)—survey protocols. Environment and Natural Resources, Government of Northwest Territories
Gross AO (1927) The snowy owl migration of 1926–27. Auk 44:479–493
Gross AO (1931) Snowy owl migration 1930–31. Auk 48:501–511
Gross AO (1947) Cyclic invasions of the snowy owl and the migration of 1945–1946. Auk 64:584–601
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
Gruyer N, Gauthier G, Berteaux D (2010) Demography of two lemming species on Bylot Island, Nunavut, Canada. Polar Biol 33:725–736. doi:10.1007/s00300-009-0746-7
Hilbe JM (2011) Negative binomial regression. Cambridge University Press, New York
Hochachka WM, Wells JV, Rosenberg KV, Tessaglia-Hymes DL, Dhondt AA (1999) Irruptive migration of common redpolls. Condor 101:195–204. doi:10.2307/1369983
Holland JS (2013) Homesick owls confusing airports with arctic tundra. National Geographic 12 December 2013
Holt D, Larson MD, Smith N, Evans D, Parmelee DF (2015) The snowy owl (Bubo scandiacus). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca
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
Kaufman K (2013) Notes from a snowy owl invasion. Audubon Magazine 4 December 2013
Keith L (1963) A note on snowy owl food habits. Wilson Bull 75:276–277
Kerlinger P, Lein MR (1986) Differences in winter range among age-sex classes of snowy owls Nyctea scandiaca in North America. Ornis Scand 17:1–7. doi:10.2307/3676745
Kerlinger P, Lein MR (1988) Population ecology of snowy owls during winter on the Great Plains of North America. Condor 90:866–874. doi:10.2307/1368844
Kerlinger P, Lein MR, Sevick BJ (1985) Distribution and population fluctuations of wintering snowy owls (Nyctea scandiaca) in North America. Can J Zool 63:1829–1834. doi:10.1139/z85-273
Koenig WD, Knops JMH (2001) Seed-crop size and eruptions of North American boreal seed-eating birds. J Anim Ecol 70:609–620. doi:10.1046/j.1365-2656.2001.00516.x
Korpimäki E, Brown PR, Jacob J, Pech RP (2004) The puzzles of population cycles and outbreaks of small mammals solved? Bioscience 54:1071–1079. doi:10.1641/0006-3568(2004)054[1071:tpopca]2.0.co;2
Krebs CJ (2011) Of lemmings and snowshoe hares: the ecology of northern Canada. Proc R Soc B Biol Sci 278:481–489. doi:10.1098/rspb.2010.1992
Krebs CJ, Kenney AJ, Gilbert S, Danell K, Angerbjorn 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
Lack D (1954) The natural regulation of animal numbers. Oxford University Press, Oxford
Le Corre M, Dussault C, Côté SD (2014) Detecting changes in the annual movements of terrestrial migratory species: using the first-passage time to document the spring migration of caribou. Mov Ecol. doi:10.1186/s40462-014-0019-0
Link WA, Sauer JR (1999) Controlling for varying effort in count surveys: an analysis of Christmas Bird Count data. J Agric Biol Environ Stat 4:116–125. doi:10.2307/1400592
McCulloch CE, Searle SR (2001) Generalized, linear and mixed models. Wiley Inter-science, New York
Miller MJ, Bonhommeau S, Munk P, Castonguay M, Hanel R, McCleave JD (2015) A century of research on the larval distributions of the Atlantic eels: a re-examination of the data. Biol Rev 90:1035–1064. doi:10.1111/brv.12144
Morrissette M, Bêty J, Gauthier G, Reed A, Lefebvre J (2010) Climate, trophic interactions, density dependence and carry-over effects on the population productivity of a migratory Arctic herbivorous bird. Oikos 119:1181–1191. doi:10.1111/j.1600-0706.2009.18079.x
Newton I (1970) Finches. Collins, London
Newton I (2002) Population limitation in Holarctic owls. In: Newton I, Kavanagh R, Olson J, Taylor IR (eds) Ecology and conservation of owls. CSIRO, Collingwood, pp 3–29
Newton I (2006a) Advances in the study of irruptive migration. Ardea 94:433–460
Newton I (2006b) Movement patterns of common crossbills Loxia curvirostra in europe. Ibis 148:782–788. doi:10.1111/j.1474-919X.2006.00585.x
Newton I (2008) The migration ecology of birds. Academic Press, London
Potapov E, Sale R (2012) The snowy owl. Poyser, London
Predavec M, Krebs CJ, Danell K, Hyndman R (2001) Cycles and synchrony in the collared lemming (Dicrostonyx groenlandicus) in Arctic North America. Oecologia 126:216–224. doi:10.1007/s004420000516
Shelford VE (1945) The relation of snowy owl migration to the abundance of the collared lemming. Auk 62:592–596
Smith N (1997) Observations of wintering snowy owls (Nyctea scandiaca) at Logan Airport, East Boston, Massachusetts from 1981–1997. In: Duncan JR, Johnson DH, Nicholls TH (eds) Biology and conservation of owls of the Northern Hemisphere: 2nd International symposium. Forest Service, US Department of Agriculture, North Central Forest Experiment Station, St Paul, pp 591–596
Stenseth NC (1999) Population cycles in voles and lemmings: density dependence and phase dependence in a stochastic world. Oikos 87:427–461. doi:10.2307/3546809
Svardson G (1957) The invasion type of bird migration. Br Birds 50:314–343
Therrien JF, Gauthier G, Bêty J (2011) An avian terrestrial predator of the Arctic relies on the marine ecosystem during winter. J Avian Biol 42:363–369. doi:10.1111/j.1600-048X.2011.05330.x
Therrien JF, Gauthier G, Korpimäki E, Bêty J (2014a) Predation pressure by avian predators suggests summer limitation of small-mammal populations in the Canadian Arctic. Ecology 95:56–57. doi:10.1890/13-0458.1
Therrien JF, Gauthier G, Pinaud D, Bêty J (2014b) Irruptive movements and breeding dispersal of snowy owls: a specialized predator exploiting a pulsed resource. J Avian Biol 45:536–544. doi:10.1111/jav.00426
Therrien JF, Pinaud D, Gauthier G, Lecomte N, Bildstein KL, Bêty J (2015) Is pre-breeding prospecting behaviour affected by snow cover in the irruptive snowy owl? A test using state-space modelling and environmental data annotated via Movebank. Mov Ecol. doi:10.1186/s40462-015-0028-7
Thouless CR (1995) Long distance movements of elephants in northern Kenya. Afr J Ecol 33:321–334. doi:10.1111/j.1365-2028.1995.tb01042.x
Wikelski M, Moskowitz D, Adelman JS, Cochran J, Wilcove DS, May ML (2006) Simple rules guide dragonfly migration. Biol Lett 2:325–329. doi:10.1098/rsbl.2006.0487
Zerbini AN, Andriolo A, Heide-Jorgensen MP, Pizzorno JL, Maia YG, VanBlaricom GR, DeMaster DP, Simoes-Lopes PC, Moreira S, Bethlem C (2006) Satellite-monitored movements of humpback whales Megaptera novaeangliae in the southwest Atlantic Ocean. Mar Ecol Prog Ser 313:295–304. doi:10.3354/meps313295
Acknowledgments
We would like to thank Suzanne Carrière (Northwest Territories Government), and Kathy Dale (CBC) for providing the data sets. We also are indebted to Gaétan Daigle, David Émond, and Dominique Fauteux for statistical assistance. This study was financially supported by the Natural Sciences and Engineering Research Council of Canada, the network of centers of excellence ArcticNet, the Polar Continental Shelf Program of Natural Resources Canada, the Fonds de Recherche du Québec Nature et Technologies and EnviroNorth. Finally, this study would not have been possible without the efforts of the numerous volunteers who conducted the CBC counts. We thank them all.
Author contribution statement
J. B. originally formulated the idea; A. R. and J. F. T. conceived and designed the experiments. G. G., K. C. and J. F. T. conducted fieldwork; A. R. developed the mathematical models and performed statistical analyses; A. R., J. B. and G. G. wrote the manuscript and all other authors revised it and provided editorial advice.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Toni Laaksonen.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Robillard, A., Therrien, J.F., Gauthier, G. et al. Pulsed resources at tundra breeding sites affect winter irruptions at temperate latitudes of a top predator, the snowy owl. Oecologia 181, 423–433 (2016). https://doi.org/10.1007/s00442-016-3588-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-016-3588-3