Abstract
Responses of one species to climate change may influence the population dynamics of others, particularly in the Arctic where food webs are strongly linked. Specifically, changes to the cryosphere may limit prey availability for predators. We examined Arctic (Vulpes lagopus) and red fox (V. vulpes) population dynamics near the southern edge of the Arctic fox distribution using fur harvest records from Churchill, Manitoba, Canada between 1955 and 2012. Arctic foxes showed a declining population trend over time (inferred from harvest records corrected for trapping effort), whereas the red fox population trend was relatively stable. The positive relationship between the annual Arctic and red fox harvests suggested interspecific competition did not promote the Arctic fox decline. To investigate alternative mechanisms, we evaluated the relative influence of sea-ice phenology, snow depth, snow duration, winter thaws, and summer temperature on the harvest dynamics of both species in the most recent 32 years (1980–2012; n = 29) of our data. Arctic fox harvests were negatively related to the length of time Hudson Bay was free of sea ice. Shorter sea ice duration may reduce access to seal carrion as an alternative winter food source when lemming densities decline. Contrary to our prediction, red fox harvest was not related to summer temperature but was positively related to snow depth, suggesting winter prey availability may limit red fox population growth. Predators have an important ecological role, so understanding the influence of changes in the cryosphere on predator–prey interactions may better illuminate the broader influence of climate change on food-web dynamics.
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References
Angerbjörn A, Tannerfeldt M, Erlinge S (1999) Predator-prey relationships: arctic foxes and lemmings. J Anim Ecol 68:34–49. https://doi.org/10.1046/j.1365-2656.1999.00258.x
Audet AM, Robbins CB, Lariviere S (2002) Alopex lagopus. Mammal Sp 713:1–10. https://doi.org/10.1644/0.713.1
Bilodeau F, Gauthier G, Berteaux D (2013a) The effect of snow cover on lemming population cycles in the Canadian High Arctic. Oecologia 172:1007–1016. https://doi.org/10.1007/s00442-012-2549-8
Bilodeau F, Reid DG, Gauthier G, Krebs CJ, Berteaux D, Kenney AJ (2013b) Demographic response of tundra small mammals to a snow fencing experiment. Oikos 122:1167–1176. https://doi.org/10.1111/j.1600-0706.2012.00220.x
Boonstra R et al (2020) The stress of Arctic warming on polar bears. Glob Change Biol 26:4197–4214. https://doi.org/10.1111/gcb.1514
Brown R, Derkson C, Wang L (2010) A multi-data set analysis of variability and change in Arctic spring snow cover extent, 1967–2008. J Geophys Res 115:D16111. https://doi.org/10.1029/2010JD013975
Buchwal A, Rachlewicz G, Fonti P, Cherubini P, Gärtner H (2013) Temperature modulates intra-plant growth of Salix polaris from a high Arctic site (Svalbard). Polar Biol 36:1305–1318. https://doi.org/10.1007/s00300-013-1349-x
Callaghan TV, Johansson M, Brown RD, Groisman PY, Labba N, Radionov V et al (2011) The changing face of Arctic snow cover: a synthesis of observed and projected changes. Ambio 40:17–31. https://doi.org/10.1007/s13280-011-0212-y
Cattadori IM, Haydon DT, Thirgood SJ, Hudson PJ (2003) Are indirect measures of abundance a useful index of population density? The case of red grouse harvesting. Oikos 100:439–446. https://doi.org/10.1034/j.1600-0706.2003.12072.x
Cherry SG, Derocher AE, Thiemann GW, Lunn NJ (2013) Migration phenology and seasonal fidelity of an Arctic marine predator in relation to sea ice dynamics. J Anim Ecol 82:912–921. https://doi.org/10.1111/1365-2656.12050
Comiso JC (2012) Large decadal decline of the Arctic multiyear ice cover. J Clim 25:1176–1193. https://doi.org/10.1175/JCLI-D-11-00113.1
Descamps S, Aars J, Fuglei E, Kovacs KM, Lydersen C, Pavlova O, Pedersen ÅØ, Ravolainen V, Strøm H (2017) Climate change impacts on wildlife in a high Arctic archipelago—Svalbard, Norway. Glob Change Biol 23:490–502. https://doi.org/10.1111/gcb.13381
Dorendorf RR, Fix PJ, Prugh LR (2016) Motivation of fur trappers in interior Alaska. Hum Dimen Wildl 21:522–537. https://doi.org/10.1080/10871209.2016.1193922
Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46. https://doi.org/10.1111/j.1600-0587.2012.07348.x
Dredge LA (1992) Field guide to the Churchill region, Manitoba. Geol Surv Can Misc Rep 53:1–52
Duchesne D, Gauthier G, Berteaux D (2011) Habitat selection, reproduction and predation of wintering lemmings in the Arctic. Oecologia 167:967–980. https://doi.org/10.1007/s00442-011-2045-6
Dudenhoeffer M, Roth JD, Johnson LK, Petersen SD (2021) Arctic fox winter dietary response to damped lemming cycles estimated from fecal DNA. J Mammal 102:1455–1465. https://doi.org/10.1093/jmammal/gyab115
Ehrich D, Schmidt NM, Gauthier G, Alisauskas R, Angerbjörn A, Clark K, Ecke F, Eide NE, Framstad E, Frandsen J, Franke A, Gilg O, Giroux M, Henttonen H, Hornfeldt B, Ims RA, Kataev GD, Kharitonov SP, Killengreen ST, Krebs CJ, Lanctot RB, Lecomte N, Menyushina IE, Morris DW, Morrisson G, Oksanen L, Oksanen OIJ, Pokrovsky IG, Popov IY, Reid D, Roth JD, Saalfeld ST, Samelius G, Sittler B, Sleptsov SM, Smith PA, Sokolov AA, Sokolova NA, Soloviev MY, Solovyeva DV (2020) Documenting lemming population change in the Arctic: can we detect trends? Ambio 49:786–800. https://doi.org/10.1007/s13280-019-01198-7
Eide NE, Stien A, Prestrud P, Yoccoz NG, Fuglei E (2012) Reproductive responses to spatial and temporal prey availability in a coastal Arctic fox population. J Anim Ecol 81:640–648. https://doi.org/10.1111/j.1365-2656.2011.01936.x
Elmhagen B, Tannerfeldt M, Angerbjörn A (2002) Food-niche overlap between arctic and red foxes. Can J Zool 80:1274–1285. https://doi.org/10.1139/z02-108
Elmhagen B, Berteaux D, Burgess RM, Ehrich D, Gallant D, Henttonen H et al (2017) Homage to Hersteinsson and Macdonald: climate warming and resource subsidies cause red fox range expansion and Arctic fox decline. Polar Res 36:3
Environment Canada (2022) Station results—historical data. https://climate.weather.gc.ca/historical_data/search_historic_data_stations_e.html?searchType=stnName&timeframe=1&txtStationName=Churchill&searchMethod=contains&optLimit=yearRange&StartYear=1840&EndYear=2023&Year=2023&Month=1&Day=6&selRowPerPage=25. Accessed 28 Nov 2022
Fauteux D, Gauthier G, Berteaux D (2015) Seasonal demography of a cyclic lemming population in the Canadian Arctic. J Anim Ecol 84:1412–1422. https://doi.org/10.1111/1365-2656.12385
Frafjord K, Becker D, Angerbjörn A (1989) Interactions between Arctic and red foxes in Scandinavia—predation and aggression. Arctic 42:354–356. https://doi.org/10.14430/arctic1677
Friesen OC, Roth JD, Graham LC (2015) Sex-biased parasitism in the monogamous arctic fox driven by diet. J Mammal 96:417–424. https://doi.org/10.1093/jmammal/gyv043
Fuglei E, Ims RA (2008) Global warming and effects on the arctic fox. Sci Prog 91:175–191. https://doi.org/10.3184/003685008X327
Gagnon AS, Gough WA (2005) Trends in the dates of ice freeze-up and breakup over Hudson Bay, Canada. Arctic 58:370–382. https://doi.org/10.14430/arctic451
Gallant D, Sough BG, Reid DG, Berteaux D (2012) Arctic fox versus red fox in the warming Arctic: four decades of den surveys in north Yukon. Polar Biol 35:1421–1431. https://doi.org/10.1007/s00300-012-1181-8
Gallant D, Lecomte N, Berteaux D (2020) Disentangling the relative influences of global drivers of change in biodiversity: a study of the twentieth-century red fox expansion into the Canadian Arctic. J Anim Ecol 89:565–576. https://doi.org/10.1111/1365-2656.13090
Gharajehdaghipour T, Roth JD, Fafard PM, Markham JH (2016) Arctic foxes as ecosystem engineers: increased soil nutrients lead to increased plant productivity on fox dens. Sci Rep 6:24020. https://doi.org/10.1038/srep24020
Gliwicz J, Jancewicz E (2016) Cascade effect of climate warming: snow duration—vole population dynamics—biodiversity. Int J Environ Clim Change 6:43–52. https://doi.org/10.9734/BJECC/2016/25313
Huang J, Zhang X, Zhang Q, Lin Y, Hao M, Luo Y, Zhao Z, Yao Y, Chen X, Wang L, Nie S, Yin Y, Xu Y, Zhang J (2017) Recently amplified arctic warming has contributed to a continual global warming trend. Nat Clim Change 7:875–879. https://doi.org/10.1038/s41558-017-0009-5
Johnson-Bice SM, Roth JD, Markham JK (2022) A cosmic view of ‘tundra gardens’: satellite imagery provides a landscape-scale perspective of Arctic fox ecosystem engineering. bioRxiv. https://doi.org/10.1101/2022.08.23.504941
Jonasson S, Michelsen A, Schmidt IK, Nielsen EV (1999) Responses in microbes and plants to changed temperature, nutrient, and light regimes in the Arctic. Ecology 80:1828–1843. https://doi.org/10.1890/0012-9658(1999)080[1828:RIMAPT]2.0.CO;2
Kausrud KL, Mysterud A, Steen H, Vik JO, Østbye E, Cazelles B, Framstad E, Eikeset AM, Mysterud I, Solhøy T, Stenseth NC (2008) Linking climate change to lemming cycles. Nature 456:93–97. https://doi.org/10.1038/nature07442
Killengreen ST, Lecomte N, Ehrich D, Schott T, Yoccoz NG, Ims RA (2011) The importance of marine vs. human-induced subsidies in the maintenance of an expanding mesocarnivore in the arctic tundra. J Anim Ecol 80:1049–1060. https://doi.org/10.1111/j.1365-2656.2011.01840.x
Lai S, Warret Rodrigues C, Gallant D, Roth JD, Berteaux D (2022) Red foxes at their northern edge: competition with the Arctic fox and winter movements. J Mammal 103:586–597. https://doi.org/10.1093/jmammal/gyab164
Lunn NJ, Servanty S, Regehr EV, Converse SJ, Richardson E, Stirling I (2016) Demography of an apex predator at the edge of its range: impacts of changing sea ice on polar bears in Hudson Bay. Ecol Appl 26:1302–1320. https://doi.org/10.1890/15-1256
Macpherson AH (1969) The dynamics of Canadian arctic fox populations. Can Wildl Serv Rep Ser 8:1–52
Madsen J, Tamstorf M, Klaassen M, Eide N, Glahder C, Rigét F, Nyegaard H, Cottaar F (2007) Effects of snow cover on the timing and success of reproduction in high-Artic pink-footed geese (Anser brachyrhynchus). Polar Biol 30:1363–1372. https://doi.org/10.1007/s00300-007-0296-9
McDonald RS, Roth JD, Baldwin FB (2017) Goose persistence in fall strongly influences Arctic fox diet, but not reproduction, in the southern Arctic. Polar Res 36(sup1):5. https://doi.org/10.1080/17518369.2017.1324652
Moizan A, Warret Rodrigues C, Roth JD (2022) Different selection criteria may relax competition for denning sites between sympatric predators on the low-Arctic tundra. Res Sq. https://doi.org/10.21203/rs.3.rs-2219312/v1
Nater CR, Eide NE, Pedersen ÅØ, Yoccoz NG, Fuglei E (2021) Contributions from terrestrial and marine resources stabilize predator populations in a rapidly changing climate. Ecosphere 12:e03546. https://doi.org/10.1002/ecs2.3546
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. https://doi.org/10.1038/nature01286
Post E, Forchhammer MC, Bret-Harte MS, Callaghan TV, Christensen TR, Elberling B et al (2009) Ecological dynamics across the Arctic associated with recent climate change. Science 325:1355–1358. https://doi.org/10.1126/science.1173113
Pruitt WO Jr (1970) Some ecological aspects of snow. Ecology of the Subarctic regions. UNESCO, Paris, pp 83–100
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Reed ET, Gauthier G, Giroux JF (2004) Effects of spring conditions on breeding propensity of Greater Snow Goose females. Anim Biodiv Conserv 27(1):35–46
Ritchie JC (1957) The vegetation of northern Manitoba II: a prisere on the Hudson Bay lowlands. Ecology 38:429–435. https://doi.org/10.2307/1929886
Rodnikova A, Ims RA, Sokolov A, Skogstad G, Sokolov V, Shtro V et al (2011) Red fox takeover of Arctic fox breeding den: an observation from Yamal Peninsula, Russia. Polar Biol 34:1609–1614. https://doi.org/10.1007/s00300-011-0987-0
Roth JD (2002) Temporal variability in Arctic fox diet as reflected in stable-carbon isotopes; the importance of sea ice. Oecologia 133:70–77. https://doi.org/10.1007/s00442-002-1004-7
Roth JD (2003) Variability in marine resources affects Arctic fox population dynamics. J Anim Ecol 72:668–676. https://doi.org/10.1046/j.1365-2656.2003.00739.x
Rouse WR (1991) Impacts of Hudson Bay on the terrestrial climate of the Hudson Bay Lowlands. Arct Antarct Alp Res 1:24–30. https://doi.org/10.2307/1551433
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. https://doi.org/10.1126/science.287.5459.1770
Samelius G, Alisauskas RT (2017) Components of population growth for Arctic foxes at a large Arctic goose colony: the relative contributions of adult survival and recruitment. Polar Res 36(sup1):6. https://doi.org/10.1080/17518369.2017.1332948
Scott PA, Fayle DCF, Bentley CV, Hansell RIC (1988) Large-scale changes in atmospheric circulation interpreted from patterns of tree growth at Churchill, Manitoba, Canada. Arct Alp Res 20:199–211. https://doi.org/10.1080/00040851.1988.12002665
Shelford VE (1943) The abundance of the collared lemming (Dicrostonyx groenlandicus (TR) VAR. Richardsoni Mer.) in the Churchill Area, 1929–1940. Ecology 24:472–484. https://doi.org/10.2307/1930558
Smith TG (1976) Predation of ringed seal pups (Phoca hispida) by the arctic fox (Alopex lagopus). Can J Zool 54:1610–1616. https://doi.org/10.1139/z76-188
Statistics Canada (2022) Consumer price indexes for Canada, monthly (V41690973 series). https://www.bankofcanada.ca/rates/related/inflation-calculator/. Accessed 25 Jul 2022
Stirling I, McEwan EH (1975) The caloric value of whole ringed seals (Phoca hispida) in relation to polar bear (Ursus maritimus) ecology and hunting behavior. Can J Zool 53:1021–1027. https://doi.org/10.1139/z75-117
Stirling I, Parkinson CL (2006) Possible effects of climate warming on selected populations of polar bears (Ursus maritimus) in the Canadian Arctic. Arctic 59:261–275. https://doi.org/10.14430/arctic312
Sturm M, Schimel J, Michaelson G, Welker JM, Oberbauer SF, Liston GE, Fahnestock J, Romanovsky VE (2005) Winter biological processes could help convert arctic tundra to shrubland. Bioscience 55:17–26. https://doi.org/10.1641/0006-3568(2005)055[0017:WBPCHC]2.0.CO;2
Tang Q, Zhang X, Francis JA (2014) Extreme summer weather in northern mid-latitudes linked to a vanishing cryosphere. Nat Clim Change 4:45–50. https://doi.org/10.1038/nclimate2065
Tannerfeldt M, Angerbjörn A (1998) Fluctuating resources and the evolution of litter size in the Arctic fox. Oikos 83:545–559. https://doi.org/10.2307/3546681
Tannerfeldt M, Angerbjörn A, Arvidson B (1994) The effect of summer feeding on juvenile Arctic fox survival: a field experiment. Ecography 17:88–96. https://doi.org/10.1111/j.1600-0587.1994.tb00080.x
Tannerfeldt M, Elmhagen B, Angerbjörn A (2002) Exclusion by interference competition? The relationship between red and Arctic foxes. Oecologia 132:213–220. https://doi.org/10.1007/s00442-002-0967-8
Tarroux A, Bety J, Gauthier G, Berteaux D (2012) The marine side of a terrestrial carnivore: intra-population variation in use of allochthonous resources by arctic foxes. PLoS ONE. https://doi.org/10.1371/journal.pone.0042427
Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205. https://doi.org/10.1038/nature05429
Wapenaar W, de Bie F, Johnston D, O’Handley RM, Barkema HW (2012) Population structure of harvested red foxes (Vulpes vulpes) and coyotes (Canis latrans) on Prince Edward Island, Canada. Can Field-Nat 126:288–294. https://doi.org/10.22621/cfn.v126i4.1374
Warret Rodrigues C (2022) Use of space and resources by red foxes and Arctic foxes in a coastal tundra transitional ecosystem. PhD dissertation, University of Manitoba, Winnipeg, Manitoba, Canada
Woo MK, Ohmura A (1997) The arctic islands. In: Bailey WG, Oke T, Rouse WR (eds) The surface climates of Canada. McGill-Queen’s University Press, Montreal, pp 172–197
Wood SN (2003) Thin plate regression splines. J R Stat Soc: Ser B (stat Methodol) 65:95–114. https://doi.org/10.1111/1467-9868.00374
Wood SN (2011) Fast stable restricted maximum likelihood and marginal likelihood estimation of semiparametric generalized linear models. J R Stat Soc: Ser B (stat Methodol) 73:3–36. https://doi.org/10.1111/j.1467-9868.2010.00749.x
Zhao ST, Johnson-Bice SM, Roth JD (2022) Foxes engineer hotspots of wildlife activity on the nutrient-limited Arctic tundra. Glob Ecol Conserv. https://doi.org/10.1016/j.gecco.2022.e02310
Acknowledgements
We thank Dean Berezanski and Manitoba’s Wildlife Branch for providing fox harvest information, including the number of permits issued and pelt prices. We also thank John Markham and LeeAnn Fishback for their suggestions on previous drafts of the manuscript, and Alex Roth for creating the conceptual diagram.
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Funding was provided by the Natural Sciences and Engineering Research Council of Canada (Discovery grant 386704).
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JV conceived the study and led the writing, SJB led the statistical analysis, and JR provided supervisory input at all stages. All authors contributed to data interpretations and final revisions of the manuscript.
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Verstege, J.S., Johnson-Bice, S.M. & Roth, J.D. Arctic and red fox population responses to climate and cryosphere changes at the Arctic’s edge. Oecologia 202, 589–599 (2023). https://doi.org/10.1007/s00442-023-05418-6
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DOI: https://doi.org/10.1007/s00442-023-05418-6