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. 2019 Jul 29;14(4):327–340. doi: 10.1111/1749-4877.12388

Voles and weasels in the boreal Fennoscandian small mammal community: what happens if the least weasel disappears due to climate change?

Hannu YLÖNEN 1,, Marko HAAPAKOSKI 1, Thorbjörn SIEVERT 1, Janne SUNDELL 2
PMCID: PMC6772078  PMID: 30811858

Abstract

Climate change, habitat loss and fragmentation are major threats for populations and a challenge for individual behavior, interactions and survival. Predator–prey interactions are modified by climate processes. In the northern latitudes, strong seasonality is changing and the main predicted feature is shortening and instability of winter. Vole populations in the boreal Fennoscandia exhibit multiannual cycles. High amplitude peak numbers of voles and dramatic population lows alternate in 3–5‐year cycles shortening from North to South. One key factor, or driver, promoting the population crash and causing extreme extended lows, is suggested to be predation by the least weasel. We review the arms race between prey voles and weasels through the multiannual density fluctuation, affected by climate change, and especially the changes in the duration and stability of snow cover. For ground‐dwelling small mammals, snow provides thermoregulation and shelter for nest sites, and helps them hide from predators. Predicted increases in the instability of winter forms a major challenge for species with coat color change between brown summer camouflage and white winter coat. One of these is the least weasel, Mustela nivalis nivalis. Increased vulnerability of wrong‐colored weasels to predation affects vole populations and may have dramatic effects on vole dynamics. It may have cascading effects on other small rodent–predator interactions and even on plant–animal interactions and forest dynamics.

Keywords: cascading effects, climate change, least weasel, population cycles, predator–prey


 

Cite this article as:

Ylönen H, Haapakoski M, Sievert T, Sundell J (2019). Voles and weasels in the boreal Fennoscandian small mammal community: what happens if the least weasel disappears due to climate change? Integrative Zoology 14, 327–40.

REFERENCES

  1. Altendorf KB, Laundré JW, López González CA et al (2001). Assessing effects of predation risk on foraging behavior of mule deer. Journal of Mammalogy 82, 430–9. [Google Scholar]
  2. Andersson M, Erlinge S (1977). Influence of predation on rodent populations. Oikos 29, 591–7. [Google Scholar]
  3. 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. [DOI] [PubMed] [Google Scholar]
  4. Apfelbach R, Blanchard CD, Blanchard RJ et al (2005). The effects of predator odors in mammalian prey species: A review of field and laboratory studies. Neuroscience & Biobehavioral Reviews 29, 1123–44. [DOI] [PubMed] [Google Scholar]
  5. Apfelbach R, Parsons MH, Soini HA et al (2015). Are single odorous components of a predator sufficient to elicit defensive behaviors in prey species? Frontiers in Neuroscience 9, 263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Apps PJ, Weldon PJ, Kramer M (2015). Chemical signals in terrestrial vertebrates: Search for design features. Natural Product Reports 32, 1131–53. [DOI] [PubMed] [Google Scholar]
  7. Atmeh K, Andruszkiewicz A, Zub K (2018). Climate change is affecting mortality of weasels due to camouflage mismatch. Scientific Reports 8, 7648. doi: 10.1038/s41598-018-26057-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Beale MH, Birkett MA, Bruce TJA et al (2006). Aphid alarm pheromone produced by transgenic plants affects aphid and parasitoid behavior. Proceedings of the National Academy of Sciences. National Academy of Sciences 103, 10509–13. [DOI] [PMC free article] [PubMed]
  9. Bedoya-Perez MA, Carthey AJR, Mella VSA et al (2013). A practical guide to avoid giving up on giving-up densities. Behavioral Ecology and Sociobiology 67, 1541–53. [Google Scholar]
  10. Bleicher SS, Marko H, Morin DJ et al (2019). Balancing food, activity and the dangers of sunlit nights. Behavioral Ecology and Sociobiology 73, 95 10.1007/s00265-019-2703-y [DOI] [Google Scholar]
  11. Boissy A, Terlouw C, Le Neindre P (1998). Presence of cues from stressed conspecifics increases reactivity to aversive events in cattle: Evidence for the existence of alarm substances in urine. Physiology and Behavior 63, 489–95. [DOI] [PubMed] [Google Scholar]
  12. Bowers W, Nault L, Webb R (1972). Aphid alarm pheromone: Isolation, identification, synthesis. Science 177, 1–2. [DOI] [PubMed] [Google Scholar]
  13. Brechbühl J, Moine F, Klaey M et al (2013). Mouse alarm pheromone shares structural similarity with predator scents. Proceedings of the National Academy of Sciences 110, 4762–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Breed MD, Guzmán-Novoa E, Hunt GJ (2004). Defensive behavior of honey bees: Organization, genetics, and comparisons with other bees. Annual Review of Entomology. Annual Reviews 49, 271–98. [DOI] [PubMed] [Google Scholar]
  15. Brinck C, Erlinge S, Sandell M (1983). Anal sac secretion in mustelids a comparison. Journal of Chemical Ecology 9, 727–45. [DOI] [PubMed] [Google Scholar]
  16. Brown JS (1988). Patch use as an indicator of habitat preference, predation risk, and competition. Behavioral Ecology and Sociobiology 22, 37–47. [Google Scholar]
  17. Brown JS, Alkon PU (1990). Testing values of crested porcupine habitats by experimental food patches. Oecologia 83, 512–8. [DOI] [PubMed] [Google Scholar]
  18. Brown JS, Kotler BP, Bouskila A (2001). Ecology of fear: Foraging games between predators and prey with pulsed resources. Annales Zoologici Fennici 38, 71–87. [Google Scholar]
  19. Bytheway JP, Carthey AJR, Banks PB (2013). Risk vs. reward: How predators and prey respond to aging olfactory cues. Behavioral Ecology and Sociobiology 67, 715–25. [Google Scholar]
  20. Cornulier T, Yoccoz NG, Bretagnolle V et al (2013). Europe-wide dampening of population cycles in keystone herbivores. Science 340, 63–6. [DOI] [PubMed] [Google Scholar]
  21. Duffield KR, Bowers EK, Sakaluk SK et al (2017). A dynamic threshold model for terminal investment. Behavioral Ecology and Sociobiology 71, 185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ecke F, Christensen P, Sandström P et al (2006). Identification of landscape elements related to local declines of a boreal grey-sided vole population. Landscape Ecology 21, 485–97. [Google Scholar]
  23. Erlinge S, Sandell M (1986). Seasonal changes in the social organization of male stoats, Mustela erminea: An Effect of shifts between two decisive resources. Oikos 47, 57–62. [Google Scholar]
  24. Erlinge S, Sandell M, Brinck C (1982). Scent-marking and its territorial significance in stoats, Mustela erminea. Animal Behaviour 30, 811–8. [Google Scholar]
  25. Forbes KM, Henttonen H, Hirvelä-Koski V et al (2015). Food provisioning alters infection dynamics in populations of a wild rodent. Proceedings of the Royal Society B 282, 20151939. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Fuelling O, Halle S (2004). Breeding suppression in free-ranging grey-sided voles under the influence of predator odour. Oecologia 138, 151–9. [DOI] [PubMed] [Google Scholar]
  27. Gehring TM, Swihart RK (2004). Home range and movements of long-tailed weasels in a landscape fragmented by agriculture. Journal of Mammalogy 85, 79–86. [Google Scholar]
  28. Gillingham BJ (1984). Meal size and feeding rate in the least weasel (Mustela nivalis). Journal of Mammalogy 65, 517–9. [Google Scholar]
  29. Gomes LAP, Salgado PMP, Barata EN et al (2013). Alarm scent-marking during predatory attempts in the Cabrera vole (Microtus cabrerae Thomas, 1906). Ecological Research 28, 335–43. [Google Scholar]
  30. Haapakoski M, Sundell J, Ylönen H (2012). Predation risk and food: Opposite effects on overwintering survival and onset of breeding in a boreal rodent: Predation risk, food and overwintering. Journal of Animal Ecology 81, 1183–92. [DOI] [PubMed] [Google Scholar]
  31. Haapakoski M, Sundell J, Ylönen H (2013). Mammalian predator–prey interaction in a fragmented landscape: Weasels and voles. Oecologia 173, 1227–35. [DOI] [PubMed] [Google Scholar]
  32. Haapakoski M, Sundell J, Ylönen H (2015). Conservation implications of change in antipredator behavior in fragmented habitat: Boreal rodent, the bank vole, as an experimental model. Biological Conservation 184, 11–7. [Google Scholar]
  33. Haapakoski M, Hardenbol AA, Matson KD (2018). Exposure to chemical cues from predator-exposed conspecifics increases reproduction in a wild rodent. Scientific Reports 8, 17214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hanski I, Hansson L, Henttonen H (1991). Specialist predators, generalist predators, and the microtine rodent cycle. The Journal of Animal Ecology 60, 353–67. [Google Scholar]
  35. Hanski I, Henttonen H, Korpimäki E, Oksanen L, Turchin P (2001). Small-rodent dynamics and predation. Ecology 82, 1505–20. [Google Scholar]
  36. Hanski I, Turchin P, Korpimäki E et al (1993). Population oscillations of boreal rodents: Regulation by mustelid predators leads to chaos. Nature 364, 232–5. [DOI] [PubMed] [Google Scholar]
  37. Hansson L, Henttonen H (1985). Gradients in density variations of small rodents: The importance of latitude and snow cover. Oecologia 67, 394–402. [DOI] [PubMed] [Google Scholar]
  38. Hartman EJ, Abrahams MV (2000). Sensory compensation and the detection of predators: The interaction between chemical and visual information. Proceedings of the Royal Society B: Biological Sciences 267, 571–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Hegab IM, Jin Y, Ye M et al (2014). Defensive responses of Brandt's voles (Lasiopodomys brandtii) to stored cat feces. Physiology & Behavior 123, 193–9. [DOI] [PubMed] [Google Scholar]
  40. Henttonen H (2000). Long-term dynamics of the bank vole Clethrionomys glareolus at Pallasjärvi, Northern Finnish taiga. Polish Journal of Ecology 48, 87–96. [Google Scholar]
  41. Henttonen H, Oksanen T, Jortikka A et al (1987). How much do weasels shape microtine cycles in the Northern Fennoscandian taiga? Oikos 50, 353–65. [Google Scholar]
  42. Hörnfeldt B, Hipkiss T, Eklund U (2005). Fading out of vole and predator cycles? Proceedings of the Royal Society B 272, 2045–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Howe N, Sheikh Y (1975). Anthopleurine: A sea anemone alarm pheromone. Science 189, 386–8. [DOI] [PubMed] [Google Scholar]
  44. Huitu O, Koivula M, Korpimäki E et al (2003). Winter food supply limits growth of northern vole populations in the absence of predation. Ecology 84, 2108–18. [Google Scholar]
  45. Hutchison VH, Marvin GA (1995). Avoidance response by adult newts (Cynops Pyrrhogaster and Notophthalmus Viridescens) to chemical alarm cues. Behaviour 132, 95–105. [Google Scholar]
  46. Jacob J, Brown JS (2000). Microhabitat use, giving-up densities and temporal activity as short- and long-term anti-predator behaviors in common voles. Oikos 91, 131–8. [Google Scholar]
  47. Järvinen A (1985). Predation causing extended low densities in microtine cycles: Implications from predation on hole-nesting passerines. Oikos 45, 157–8. [Google Scholar]
  48. Jędrzejewska B, Jędrzejewski W (1989). Seasonal surplus killing as hunting strategy of the weasel Mustela nivalis – Test of a hypothesis. Acta Theriologica 34, 347–59. [Google Scholar]
  49. Kiyokawa Y, Kikusui T, Takeuchi Y, Mori Y (2004). Alarm pheromones with different functions are released from different regions of the body surface of male rats. Chemical Senses 29, 35–40. [DOI] [PubMed] [Google Scholar]
  50. Korpela K, Helle P, Henttonen H et al (2014). Predator–vole interactions in northern Europe: The role of small mustelids revised. Proceedings of the Royal Society B 281, 20142119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Korpimäki E, Norrdahl K (1989). Avian predation on mustelids in Europe 1: Occurrence and effects on body size variation and life traits. Oikos 55, 205–15. [Google Scholar]
  52. Korpimäki E, Norrdahl K, Rinta-Jaskari T (1991). Responses of stoats and least weasels to fluctuating food abundances: Is the low phase of the vole cycle due to mustelid predation? Oecologia 88, 552–61. [DOI] [PubMed] [Google Scholar]
  53. Korpimäki E, Norrdahl K, Valkama J (1994). Reproductive investment under fluctuating predation risk: Microtine rodents and small mustelids. Evolutionary Ecology 8, 357–68. [Google Scholar]
  54. Koskela E, Ylönen H (1995). Suppressed breeding in the field vole (Microtus agrestis): An adaptation to cyclically fluctuating predation risk. Behavioral Ecology 6, 311–5. [Google Scholar]
  55. Kotler BP, Gross JE, Mitchell WA (1994). Applying patch use to assess aspects of foraging behavior in Nubian ibex. The Journal of Wildlife Management 58, 299–307. [Google Scholar]
  56. Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A (2010). Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proceedings of the Royal Society B 277, 1469–74. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Kuwahara Y, Leal WS, Nakano Y et al (1989). Phermone study on astigmait mites: XXIII. Identification of the alarm pheromone on the acarid mite, Tyrophagus neiswanderi and species specificities of alarm pheromones among four species of the same genus. Applied Entomology and Zoology 24, 424–9. [Google Scholar]
  58. Lemke P, Ren J, Alley RB et al (2007). Observations: Changes in snow, ice and frozen ground. In: Solomon S. et al, eds. Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, UK, pp. 337–83. [Google Scholar]
  59. Lima SL, Dill LM (1990). Behavioral decisions made under the risk of predation: A review and prospectus. Canadian Journal of Zoology 68, 619–40. [Google Scholar]
  60. Macdonald D (1995). European Mammals. Evolution and Behaviour. HarperCollins Publishers, London. [Google Scholar]
  61. Magnusson M, Bergsten A, Ecke F et al (2013). Predicting grey-sided vole occurrence in northern Sweden at multiple spatial scales. Ecology and Evolution 3, 4365–76. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Magurran AE, Irving PW, Henderson PA (1996). Is there a fish alarm pheromone? A wild study and critique. Proceedings of the Royal Society of London B 263, 1551–6. [Google Scholar]
  63. Mäkeläinen S, Trebatická L, Sundell J et al (2014). Different escape tactics of two vole species affect the success of the hunting predator, the least weasel. Behavioral Ecology and Sociobiology 68, 31–40. [Google Scholar]
  64. Mappes T, Ylönen H (1997). Reproductive effort of female bank voles in a risky environment. Evolutionary Ecology 11, 591–8. [Google Scholar]
  65. Mappes T, Halonen M, Suhonen J et al (1993). Selective avian predation on a population of the field vole, Microtus agrestis: Greater vulnerability of males and subordinates. Ethology Ecology & Evolution 5, 519–27. [Google Scholar]
  66. May RM (1973). Complexity and Stability in Model Ecosystems. Princeton University Press, Princeton, New Jersey, USA. [Google Scholar]
  67. Millon A, Petty SJ, Little B et al (2014). Dampening prey cycle overrides the impact of climate change on predator population dynamics: A long-term demographic study on tawny owls. Global Change Biology 20, 1770–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Mills LS, Bragina EV, Kumar AV et al (2018). Winter color polymorphisms identify global hot spots for evolutionary rescue from climate change. Science 359, 1033–6. [DOI] [PubMed] [Google Scholar]
  69. Nevo O, Orts Garri R, Hernandez Salazar LT et al (2015). Chemical recognition of fruit ripeness in spider monkeys (Ateles geoffroyi). Scientific Reports 5, 14895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  70. Norrdahl K, Korpimäki E (1995). Mortality factors in a cyclic vole population. Proceedings of the Royal Society B: Biological Sciences 261, 49–53. [DOI] [PubMed] [Google Scholar]
  71. Oksanen T, Oksanen L, Fretwell SD (1985). Surplus killing in the hunting strategy of small predators. The American Naturalist 126, 328–46. [Google Scholar]
  72. Penczykowski RM, Conolly BM, Barteon BT (2017). Winter is changing: Trophic interactions under altered snow regimes. Food Webs 13, 80–91. [Google Scholar]
  73. Sánchez-González B, Planillo A, Navarro-Castilla Á et al (2018). The concentration of fear: Mice's behavioural and physiological stress responses to different degrees of predation risk. The Science of Nature 105, 16. [DOI] [PubMed] [Google Scholar]
  74. Sievert T, Laska M (2016). Behavioral responses of CD-1 Mice to six predator odor components. Chemical Senses 41, 399–406. [DOI] [PubMed] [Google Scholar]
  75. Sievert T, Haapakoski M, Palme R, Voipio H (2019). Secondhand horror: effects of direct and indirect predator cues on behavior and reproduction of the bank vole. Ecosphere 10, e02765. [Google Scholar]
  76. Solheim R (1984). Caching behaviour, prey choice and surplus killing by pymy owls Glaucidiumpasserinum during winter, a functional response of a generalist predator. Annales Zoologici Fennici 21, 301–8. [Google Scholar]
  77. Stenseth NC (1999). Population cycles in voles and lemmings: Density dependence and phase dependence in a stochastic world. Oikos 87, 427–61. [Google Scholar]
  78. Stephens DW, Brown JS, Ydenberg RC, eds (2007). Foraging: Behavior and Ecology. University of Chicago Press, Chicago, IL. [Google Scholar]
  79. Sundell J (2003). Reproduction of the least weasel in captivity: Basic observations and the influence of food availability. Acta Theriologica 48, 59–72. [Google Scholar]
  80. Sundell J, Ylönen H (2004). Behaviour and choice of refuge by voles under predation risk. Behavioral Ecology and Sociobiology 56, 263–69. [Google Scholar]
  81. Sundell J, Ylönen H (2008). Specialist predator in a multi-species prey community: Boreal voles and weasels. Integrative Zoology 3, 51–63. [DOI] [PubMed] [Google Scholar]
  82. Sundell J, Norrdahl K, Korpimaki E et al (2000). Functional response of the least weasel, Mustela nivalis nivalis. Oikos 90, 501–8. [Google Scholar]
  83. Sundell J, Trebatická L, Oksanen T et al (2008). Predation on two vole species by a shared predator: antipredatory response and prey preference. Population Ecology 50, 257–66. [Google Scholar]
  84. Sundell J, O'Hara RB, Helle P et al (2013). Numerical response of small mustelids to vole abundance: delayed or not? Oikos 122, 1112–20. [Google Scholar]
  85. Terraube J, Villers A, Ruffino L et al (2015). Coping with fast climate change in northern ecosystems: mechanisms underlying the population-level response of a specialist avian predator. Ecography 38, 690–9. [Google Scholar]
  86. Trebatická L, Suortti P, Sundell J et al (2012). Predation risk and reproduction in the bank vole. Wildlife Research 39, 463–8. [Google Scholar]
  87. Turchin P, Batzli GO (2001). Availability of food and the population dynamics of arvicoline rodents. Ecology 82, 1521–34. [Google Scholar]
  88. Viney ME, Franks NR (2004). Is dauer pheromone of Caenorhabditis elegans really a pheromone? Naturwissenschaften 91, 123–4. [DOI] [PubMed] [Google Scholar]
  89. von Frisch K (1938). Zur Psychologie des Fisch-Schwarmes. Naturwissenschaften 26, 601–6. [Google Scholar]
  90. Wedekind C, Bettens F, Chapuisat M et al (2000). Examples of MHC-correlated sexual selection in mice and humans. In: Espmark Y, Amundsen T, Rosenqvist G, eds. Animal Signals: Signalling and Signal Design in Animal Communication. Tapir Academic Press, Trondheim, Norway, pp. 437–44. [Google Scholar]
  91. Weiß BM, Marcillo A, Manser M et al (2018). A non-invasive method for sampling the body odour of mammals. Methods in Ecology and Evolution 9, 420–9. [Google Scholar]
  92. Ylönen H (1988). Diel activity and demography in an enclosed population of the vole Clethrionomys glareolus (Schreb.). Annales Zoologici Fennici 25, 221–8. [Google Scholar]
  93. Ylönen H (1994). Vole cycles and antipredatory behaviour. Trends in Ecology & Evolution 9, 426–30. [DOI] [PubMed] [Google Scholar]
  94. Ylönen H (2001). Predator odours and behavioural responses of small rodents: An evolutionary perspective. In: Pelz HJ, Cowan PD, Feare CJ, eds. Advances in Vertebrate Pest Management II. Filander, Fuerth, pp. 123–38. [Google Scholar]
  95. Ylönen H, Brown JS (2007). Fear and the foraging, breeding, and sociality of rodents, in Wolff JO, Sherman PW, eds. Rodent Societies: An Ecological & Evolutionary Perspective. University of Chicago Press, Chicago, IL, USA, p. 610. [Google Scholar]
  96. Ylönen H, Ronkainen H (1994). Breeding suppression in the bank vole as antipredatory adaptation in a predictable environment. Evolutionary Ecology 8, 658–66. [Google Scholar]
  97. Ylönen H, Sundell J, Tiilikainen R et al (2003). Weasels’ (Mustela nivalis nivalis) preference for olfactory cues of the vole (Clethrionomys glareolus). Ecology 84, 1447–52. [Google Scholar]
  98. Ylönen H, Eccard JA, Jokinen I, Sundell J (2006). Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behavioral Ecology and Sociobiology 60, 350–8. [Google Scholar]
  99. Zimova M, Hackländer K, Good JM et al (2018). Function and underlying mechanisms of seasonal color moulting in mammals and birds: what keeps them changing in a warming world? Biological Reviews 93, 1478–98. [DOI] [PubMed] [Google Scholar]
  100. Zimova M, Mills LS, Nowak JJ (2016). High fitness costs of climate change-induced camouflage mismatch. Ecology Letters 19, 299–307. [DOI] [PubMed] [Google Scholar]

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