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The relationship between wolverine and larger predators, lynx and wolf, in a historical ecosystem context

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Abstract

Apex predators play an important role in shaping ecosystem structure. They may suppress smaller predators (mesopredators) but also subsidize scavengers via carrion provisioning. However, the importance of these interactions can change with ecosystem context. The wolverine (Gulo gulo) is a cold-adapted carnivore and facultative scavenger. It has a circumboreal distribution, where it could be either suppressed or subsidized by larger predators. In Scandinavia, the wolverine might interact with two larger predators, wolf (Canis lupus) and lynx (Lynx lynx), but human persecution decimated the populations in the nineteenth and early twentieth century. We investigated potential relationships between wolverine and the larger predators using hunting bag statistics from 15 Norwegian and Swedish counties in 1846–1922. Our best models showed a positive association between wolverine and lynx trends, taking ecological and human factors into account. There was also a positive association between year-to-year fluctuations in wolverine and wolf in the latter part of the study period. We suggest these associations could result from positive lynx–wolverine interactions through carrion provisioning, while wolves might both suppress wolverine and provide carrion with the net effect becoming positive when wolf density drops below a threshold. Wolverines could thus benefit from lynx presence and low-to-intermediate wolf densities.

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References

  • Andrén H, Persson J, Mattisson J, Danell AC (2011) Modeling the combined effect of an obligate predator and a facultative predator on a common prey: lynx Lynx lynx and wolverine Gulo gulo predation on reindeer Rangifer tarandus. Wildl Biol 17:33–43

    Article  Google Scholar 

  • Angelstam P, Lindström E, Widén P (1984) Role of predation in short-term population fluctuations of some birds and mammals in Fennoscandia. Oecologia 62:199–208

    Article  Google Scholar 

  • Angerbjörn A, Tannerfeldt M, Bjärvall A, Ericson M, From J, Norén E (1995) Dynamics of the arctic fox population in Sweden. Ann Zool Fenn 32:55–68

    Google Scholar 

  • Atwood TC, Gese EM (2008) Coyotes and recolonizing wolves: social rank mediates risk-conditional behaviour at ungulate carcasses. Anim Behav 75:753–762

    Article  Google Scholar 

  • Berger KM, Conner MM (2008) Recolonizing wolves and mesopredator suppression of coyotes: impacts on pronghorn population dynamics. Ecol Appl 18:599–612

    Article  PubMed  Google Scholar 

  • Berger J, Stacey PB, Bellis L, Johnson MP (2001) A mammalian predator–prey imbalance: grizzly bear and wolf extinction affect avian Neotropical migrants. Ecol Appl 11:946–960

    Google Scholar 

  • Bowman J, Ray JC, Magoun AJ, Johnson DS, Dawson FN (2010) Roads, logging, and the large-mammal community of an eastern Canadian boreal forest. Can J Zool 88:454–467

    Article  Google Scholar 

  • Brown RD, Brasnett B (2010) Canadian Meteorological Centre (CMC) daily snow depth analysis data. Environment Canada. National Snow and Ice Data Center, Boulder

  • Carbone C, Frame L, Frame G, Malcolm J, Fanshawe J, FitzGibbon C, Schaller G, Gordon IJ, Rowcliffe JM, Du Toit JT (2005) Feeding success of African wild dogs (Lycaon pictus) in the Serengeti: the effects of group size and kleptoparasitism. J Zool 266:153–161

    Article  Google Scholar 

  • Collett R (1911) Norges pattedyr. Aschehoug, Kristiania

    Book  Google Scholar 

  • Copeland JP, McKelvey KS, Aubry KB, Landa A, Persson J, Inman RM, Lofroth E, Golden H, Squires JR, Magoun A, Schwartz MK, Wilmot J, Copeland CL, Yates RE, Kojola I, May R (2010) The bioclimatic envelope of the wolverine (Gulo gulo): do climatic constraints limit its geographic distribution? Can J Zool 88:233–246

    Article  Google Scholar 

  • Creel S (2001) Four factors modifying the effect of competition on carnivore population dynamics as illustrated by African wild dogs. Conserv Biol 15:271–274

    Article  Google Scholar 

  • DeVault TL, Rhodes OE, Shivik JA (2003) Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos 102:225–234

    Article  Google Scholar 

  • Elmhagen B, Rushton SP (2007) Trophic control of mesopredators in terrestrial ecosystems: top-down or bottom-up? Ecol Lett 10:197–206

    Article  PubMed  Google Scholar 

  • Elmhagen B, Ludwig G, Rushton SP, Helle P, Linden H (2010) Top predators, mesopredators and their prey: interference ecosystems along bioclimatic productivity gradients. J Anim Ecol 79:785–794

    CAS  PubMed  Google Scholar 

  • Elmhagen B, Hellström P, Angerbjörn A, Kindberg J (2011) Changes in vole and lemming fluctuations in Northern Sweden 1960–2008 revealed by fox dynamics. Ann Zool Fenn 48:167–179

    Article  Google Scholar 

  • ESRI (2011) ArcGIS. Version 10. Environmental Systems Research Institute, Redlands

  • Flagstad Ø, Hedmark E, Landa A, Brøseth H, Persson J, Andersen R, Segerström P, Ellegren H (2004) Colonization history and non-invasive monitoring of a re-established wolverine population. Conserv Biol 18:676–688

    Article  Google Scholar 

  • Fox J (2002) An R and S-PLUS companion to applied regression. Sage, Thousand Oaks

    Google Scholar 

  • Fretwell SD (1977) The regulation of plant communities by food chains exploiting them. Persp Biol Med 20:169–185

    Google Scholar 

  • Gese EM, Stotts TE, Grothe S (1996) Interactions between coyotes and red foxes in Yellowstone National Park, Wyoming. J Mammal 77:377–382

    Article  Google Scholar 

  • Glen AS, Dickman CR (2005) Complex interactions among mammalian carnivores in Australia, and their implications for wildlife management. Biol Rev 80:387–401

    Article  PubMed  Google Scholar 

  • Grace JB (2008) Structural equation modeling for observational studies. J Wildl Manage 72:14–22

    Article  Google Scholar 

  • Haglund B (1966) Winter habits of the lynx (Lynx lynx L.) and wolverine (Gulo gulo L.) as revealed by tracking in the snow (In Swedish, with English summary). Viltrevy 4:81–310

    Google Scholar 

  • Hansen M, DeFries R, Townsend JRG, Sohlberg R (1998) UMD global land cover classification, 1 km, 1.0. Department of Geography, University of Maryland, College Park, Maryland, 1981–1994

  • Hellborg L, Walker CW, Rueness EK, Stacy JE, Kojola I, Valdmann H, Vilà C, Zimmermann B, Jakobsen KS, Ellegren H (2002) Differentiation and levels of genetic variation in northern European lynx (Lynx lynx) populations revealed by microsatellites and mitochondrial DNA analysis. Conserv Genet 3:97–111

    Article  CAS  Google Scholar 

  • Henden J, Ims RA, Yoccoz NG (2009) Nonstationary spatio-temporal small rodent dynamics: evidence from long-term Norwegian fox bounty data. J Anim Ecol 68:636–645

    Article  Google Scholar 

  • Hörnfeldt B (1978) Synchronous population fluctuations in voles, small game, owls, and tularemia in northern Sweden. Oecologia 32:141–152

    Article  Google Scholar 

  • Inman RM, Magoun AJ, Persson J, Mattisson J (2012) The wolverine’s niche: linking reproductive chronology, caching, competition, and climate. J Mammal 93:634–644

    Article  Google Scholar 

  • Jedrzejewski W, Schmidt K, Milkowski L, Jedrzejewska B, Okarma H (1993) Foraging by lynx and its role in ungulate mortality: the local (Bialowieza forest) and the Palearctic viewpoints. Acta Theriol 38:385–403

    Google Scholar 

  • Johnsen S (1929) Rovdyr- og rovfuglstatistikken i Norge. Berg Mus Årbok 2:1–140

    Google Scholar 

  • Kardell Ö, Dahlström A (2013) Wolves in the early nineteenth-century county of Jönköping, Sweden. Environ Hist 19:339–370

    Article  Google Scholar 

  • Krebs J, Lofroth E, Copeland J, Banci V, Cooley D, Golden H, Magoun A, Mulders R, Shults B (2004) Synthesis of survival rates and causes of mortality in North American wolverines. J Wildl Manage 68:493–502

    Article  Google Scholar 

  • Landa A, Strand O, Swenson JE, Skogland T (1997) Wolverines and their prey in southern Norway. Can J Zool 75:1292–1299

    Article  Google Scholar 

  • Linnell JD, Strand O (2000) Interference interactions, co-existence and conservation of mammalian carnivores. Divers Distrib 6:169–176

    Article  Google Scholar 

  • Mattisson J, Andrén H, Persson J, Segerström P (2011a) Influence of intraguild interactions on resource use by wolverines and Eurasian lynx. Am Soc Mammal 92:1321–1330

    Article  Google Scholar 

  • Mattisson J, Persson J, Andrén H, Segerström P (2011b) Temporal and spatial interactions between an obligate predator, the Eurasian lynx (Lynx lynx), and a facultative scavenger, the wolverine (Gulo gulo). Can J Zool 89:79–89

    Article  Google Scholar 

  • May R, van Dijk J, Wabakken P, Swenson JE, Linnell JDC, Zimmerman B, Odden J, Pedersen H, Andersen R, Landa A (2008) Habitat differentiation within the large-carnivore community of Norway’s multiple-use landscapes. J Appl Ecol 45:1382–1391

    Article  PubMed Central  PubMed  Google Scholar 

  • McLaren BE, Peterson RO (1994) Wolves, moose, and tree rings on isle royale. Science 266:1555–1558

    Article  CAS  PubMed  Google Scholar 

  • Mech LD (2007) Annual arctic wolf patch size related to arctic hare numbers. Arctic 60:309–311

    Google Scholar 

  • Mech LD, Boitani L (2003) Wolves: behavior, ecology, and conservation. University of Chicago Press, Chicago

    Book  Google Scholar 

  • Norges Offisielle Statistikk (1978) Jaktstatistikk 1846-1977 (Hunting statistics 1846–1977). Statistisk SentralByrå, Oslo

  • O’Mahoney D, Lambin X, MacKinnon JL, Coles CF (1999) Fox predation on cyclic field vole populations in Britain. Ecography 22:575–581

    Article  Google Scholar 

  • Oksanen L, Oksanen T (2000) The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–723

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Pasanen-Mortensen M, Pyykönen M, Elmhagen B (2013) Where lynx prevail, foxes will fail—limitation of a mesopredator in Eurasia. Global Ecol Biogeogr 22:868–877

    Article  Google Scholar 

  • Pasitschniak-Arts M, Larivière S (1995) Gulo gulo. Mammal Sp 499:1–10

    Google Scholar 

  • Persson J (2005) Female wolverine (Gulo gulo) reproduction: reproductive costs and winter food availability. Can J Zool 83:1453–1459

    Article  Google Scholar 

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

    Book  Google Scholar 

  • Pinheiro J, Bates D, Debroy S, Sarkar D, R Development Core Team (2012) Nlme: linear and non-linear mixed effects models. R package version 3.1-104

  • Post E, Peterson RO, Stenseth NC, McLaren BE (1999) Ecosystem consequences of wolf behavioural response to climate. Nature 401:905–907

    Article  CAS  Google Scholar 

  • Power M (1992) Top-down and bottom-up forces in food webs: do plants have primacy. Ecology 73:733–746

    Article  Google Scholar 

  • Prugh LR, Stoner SJ, Epps CW, Bean WT, Ripple WJ, Laliberte AS, Brashares JS (2009) The rise of the mesopredator. Bioscience 59:779–79

    Article  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/

  • Rausch RA (1967) Some aspects of the population ecology of wolves, Alaska. Am Zool 7:253–265

    Google Scholar 

  • Rausch A, Pearson AM (1972) Notes on the wolverine in Alaska and the Yukon territory. J Wildl Manage 36:249–268

    Article  Google Scholar 

  • Rauset GR (2013) Life and death in wolverines: Linking demography and habitat for conservation. PhD dissertation, Department of Ecology, Swedish University of Agricultural Sciences, Uppsala, Sweden

  • Ripple WJ, Larsen EJ, Renkin RA, Smith DW (2001) Trophic cascades among wolves, elk and aspen on Yellowstone National Park’s northern range. Biol Conserv 102:227–234

    Article  Google Scholar 

  • Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP, Schmitz OJ, Smith DW, Wallach AD, Wirsing AJ (2014) Status and ecological effects of the world’s largest carnivores. Science 343:1241484

    Article  PubMed  Google Scholar 

  • Rosseel Y (2012) lavaan: an R Package for structural equation modeling. J Stat Softw 48:1–36

    Google Scholar 

  • Ryd Y (2007) Ren och varg-samer berättar (Reindeer and wolf–Sami tells). Natur och Kultur, Stockholm

  • Selva N, Fortuna MA (2007) The nested structure of a scavenger community. Proc R Soc Lond 274:1101–1108

    Article  Google Scholar 

  • Smith DW, Peterson RO, Houston DB (2003) Yellowstone after wolves. Bioscience 53:330–340

    Article  Google Scholar 

  • Soule ME, Bolger DT, Alberts AC, Wright J, Sorice M, Hill S (1988) Reconstructed dynamics of rapid extinctions of chaparral-requiring birds in urban habitat islands. Conserv Biol 2:75–92

    Article  Google Scholar 

  • Svensson L, Wabakken P, Kojola I, Maartmann E, Strømseth TH, Åkesson M, Flagstad Ø, Zetterberg A (2013) The wolf in Scandinavia and Finland: final report from wolf monitoring in the 2012–2013 winter (in Swedish with English abstract). Report no. 6-2013. Hedmark University College, Norway

  • Sveriges Officiella Statistik (1850) Folkmängden i Sverige vid 1845 års slut (Sweden’s official statistics. The human population in Sweden by the end of 1845). Norstedt & Söner, Stockholm

  • Sveriges Officiella Statistik (1870-1920) Skogsväsendet. Årsberättelser (Sweden’s official statistics. Forestry. Yearly reports). Norstedt & Söner, Stockholm

  • Sveriges Officiella Statistik (1879) Skogs-styrelsen Underdåniga Berättelse angående Skogs- och Jaktväsendet i Sverige intill år 1870 (Sweden’s official statistics. The National Board of Forestry’s Humble Report on Forestry and Hunting in Sweden up until 1870). Norstedt & Söner, Stockholm

  • Sveriges Officiella Statistik (1890) Jordbruk och boskapsskötsel. Hushållningssällskapens berättelser för år 1890 (Sweden’s official statistics. Agricture and stockfarming. Tales of the housekeeping societies in 1890). Norstedt & Söner, Stockholm

  • Thompson JN (1988) Variations in interspecific interactions. Annu Rev Ecol Evol Syst 19:65–87

    Article  Google Scholar 

  • Thurber JM, Peterson RO (1993) Effects of population density and pack size on the foraging ecology of gray wolves. J Mammal 74:879–889

    Article  Google Scholar 

  • van Dijk J, Gustavsen L, Mysterud A, May R, Flagstad Ö, Brøseth H, Andersen R, Steen H, Landa A (2008) Diet shift of a facultative scavenger, the wolverine, following recolonization of wolves. J Anim Ecol 77:1183–1190

    Article  PubMed  Google Scholar 

  • Wabakken P, Sand H, Liberg O, Bjärvall A (2001) The recovery, distribution, and population dynamics of wolves on the Scandinavian peninsula, 1978–1998. Can J Zool 79:710–725

    Article  Google Scholar 

  • Wikenros C, Liberg O, Sand H, Andrén H (2010) Competition between recolonizing wolves and resident lynx in Sweden. Can J Zool 88:271–279

    Article  Google Scholar 

  • Wilmers CC, Post E (2006) Predicting the influence of wolf-provided carrion on scavenger community dynamics under climate change scenarios. Glob Change Biol 12:403–409

    Article  Google Scholar 

  • Wilmers CC, Crabtree RL, Smith DW, Murphy KM, Getz WM (2003) Trophic facilitation by introduced top predators: grey wolf subsidies to scavengers in Yellowstone National Park. J Anim Ecol 72:909–916

    Article  Google Scholar 

  • Wilson EE, Wolkovich EM (2011) Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol 26:129–135

    Article  PubMed  Google Scholar 

  • Yang W, Shabanov NV, Huang D, Wang W, Dickinson RE, Neemani RR, Knyazikhin Y, Myeni RB (2006) Analysis of leaf area index products from combination of MODIS Terra and Aqua data. Remote Sens Environ 104:297–312

    Article  Google Scholar 

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Acknowledgments

We are grateful to Ranga Myneni and Arindam Samantha who prepared and supplied us with the FPAR data. This research was funded by the Swedish Research Council Formas, the Strategic Research Programme EkoKlim at Stockholm University and the Royal Swedish Academy of Sciences. Comments from two anonymous reviewers improved the paper.

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Correspondence to Bodil Elmhagen.

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Communicated by Christopher N Johnson.

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Khalil, H., Pasanen-Mortensen, M. & Elmhagen, B. The relationship between wolverine and larger predators, lynx and wolf, in a historical ecosystem context. Oecologia 175, 625–637 (2014). https://doi.org/10.1007/s00442-014-2918-6

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