Abstract
Both the theory and the observations suggest that, there are strong links between herbivores and plants in terrestrial ecosystems; although, the effect of herbivores on plant community biomass is often attributed to variations in plant palatability. The existence of a strong link is commonly tested by constructing exclosures that exclude herbivores during a period of time. We here present data from two long-term (9 and 20 years, respectively) herbivore exclosure studies in lemming habitats on arctic tundra in northernmost Norway. The exclusion of all mammalian herbivores triggered strong increases in community level plant biomass and substantial changes in plant community composition. Palatable plants like graminoids and large bryophytes, as well as unpalatable plants like evergreen ericoids, deciduous shrubs, and lichens were all favored by excluding lemmings. These results reveal that a substantial increase in community biomass which occurs only when plant species capable of accumulating biomass are present, and palatability is a poor predictor of long-term responses of plants to excluding herbivores.
Similar content being viewed by others
References
Ahti T, Hämet-Ahti L, Jalas J. 1968. Vegetation zones and their sections in northwestern Europe. Ann Bot Fenn 5:169–211.
Aleksandrova VD, Andreev VN, Vahtina TV, Dydina RA, Kareva GI, Petrovskij VV, Šamarin VF. 1964. Kormovaja harakteristika rostennij Krajnego Severa SSSR. Moskow: Nauka.
Aunapuu M, Dahlgren J, Oksanen T, Grellmann D, Oksanen L, Olofsson J, Rammul U, Schneider M, Johansen B, Hygen HO. 2008. Spatial patterns and dynamic responses of arctic food webs corroborate the exploitation ecosystems hypothesis (EEH). Am Nat 171:249–62.
Batzli GO. 1993. Food selection by lemmings. In: Stenseth NC, Ims RA, Eds. The biology of Lemmings. London: Academic Press. p 281–301.
Batzli GO, White RG, MacLean SF, Pitelka FA, Collier BD. 1980. The herbivore-based trophic system. In: Brown J, Miller PC, Tieszen LL, Bunnell F, Eds. An arctic ecosystem: the coastal tundra at Barrow, Alaska. Stroudsburg: Dowden, Hutchinson and Ross, Inc. p 335–410.
Bond W. 2010. Consumer control by megafauna and fire. In: Terborgh J, Estes JA, Eds. Trophic cascades: predators, prey, and the changing dynamics of nature. Washington, DC: Island Press. p 275–86.
Brown J, Everett KR, Webber PJ, MacLean SF, Murray DF. 1980. The coastal tundra at Barrow. In: Brown J, Miller PC, Tieszen LL, Bunnell F, Eds. An arctic ecosystem: the coastal tundra at Barrow, Alaska. Stroudsburg: Dowden, Hutchinson & Ross, Inc. p 1–29.
Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ. 2002. Positive interactions among alpine plants increase with stress. Nature 417:844–8.
Choler P, Michalet R, Callaway RM. 2001. Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–308.
Dahlgren J, Oksanen L, Oksanen T, Olofsson J, Hamback PA, Lindgren A. 2009a. Plant defences to no avail? Responses of plants of varying edibility to food web manipulations in a low arctic scrubland. Evol Ecol Res 11:1189–203.
Dahlgren J, Oksanen L, Olofsson J, Oksanen T. 2009b. Plant defences at no cost? The recovery of tundra scrubland following heavy grazing by grey-sided voles, Myodes rufocanus. Evol Ecol Res 11:1205–16.
Gjaerevoll O. 1956. The plant communities of the Scandinavian alpine snow-beds. Trondheim: F. Bruns Bokhandel.
Gough L, Moore JC, Shaver GR, Simpson RT, Johnson DR. 2012. Above- and belowground responses of arctic tundra ecosystems to altered soil nutrients and mammalian herbivory. Ecology 93:1683–94.
Grellmann D. 2002. Plant responses to fertilization and exclusion of grazers on an arctic tundra heath. Oikos 98:190–204.
Hairston NG, Smith FE, Slobodkin LB. 1960. Community structure, population control, and competition. Am Nat 94:421–5.
Hambäck PA, Oksanen L, Ekerholm P, Lindgren A, Oksanen T, Schneider M. 2004. Predators indirectly protect tundra plants by reducing herbivore abundance. Oikos 106:85–92.
Holt RD. 1977. Predation, apparent competition, and structure of prey communities. Theor Popul Biol 12:197–229.
Johnson DR, Lara MJ, Shaver GR, Batzli GO, Shaw JD, Tweedie CE. 2011. Exclusion of brown lemmings reduces vascular plant cover and biomass in Arctic coastal tundra: resampling of a 50+ year herbivore exclosure experiment near Barrow, Alaska. Environ Res Lett 6:045507.
Kalela O. 1971. Seasonal differences in the habitats of the Norwegian lemming, Lemmus lemmus (L.) in 1959 and 1960 at Kilpisjärvi, Finnish Lapland. Ann Acad Sci Fenn A IV Biol 178:1–22.
Kalela O, Koponen T. 1971. Food consumption and movements of the Norwegian lemming in areas characterized by isolated fells. Ann Zool Fenn 8:80–4.
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 456:93–7.
McNaughton SJ. 1979. Grazing as an optimization process: grass-ungulate relationships in the Serengeti. Am Nat 113:691–703.
Moen J, Lundberg PA, Oksanen L. 1993. Lemming grazing on snowbed vegetation during a population peak, Northern Norway. Arct Alp Res 25:130–5.
Moen J, Oksanen L. 1998. Long-term exclusion of folivorous mammals in two arctic-alpine plant communities: a test of the hypothesis of exploitation ecosystems. Oikos 82:333–46.
Myllymäki A, Paasikallio A, Pankakoski E, Kanervo V. 1971. Removal experiments on small quadrats as a means of rapid assessment of the abundance of small mammals. Ann Zool Fenn 8:177–85.
Mysterud A, Yoccoz NG, Stenseth NC, Langvatn R. 2001. Effects of age, sex and density on body weight of Norwegian red deer: evidence of density-dependent senescence. Proc R Soc B Biol Sci 268:911–19.
Oksanen L. 1983. Trophic exploitation and arctic phytomass patterns. Am Nat 122:45–52.
Oksanen L, Fretwell SD, Arruda J, Niemela P. 1981. Exploitation ecosystems in gradients of primary productivity. Am Nat 118:240–61.
Oksanen L, Moen J. 1994. Species-specific plant responses to exclusion of grazers in three Fennoscandian tundra habitats. Ecoscience 1:31–9.
Oksanen L, Oksanen T. 1981. Lemmings (Lemmus lemmus) and grey-sided voles (Clethrionomys rufocanus) in interaction with their resources and predators on Finnmarksvidda, northern Norway. Rep Kevo Subarct Res Stn 17:7–31.
Oksanen L, Oksanen T. 2000. The logic and realism of the hypothesis of exploitation ecosystems. Am Nat 155:703–23.
Oksanen L, Oksanen T, Dahlgren J, Hambäck PA, Ekerholm P, Lindgren Å, Olofsson J. 2010. Islands as tests of the green world hypothesis. In: Terborgh J, Estes JA, Eds. Trophic cascades: predators, prey, and the changing dynamics of nature. Washington, DC: Island Press. p 163–77.
Oksanen L, Virtanen R. 1995. Topographic, altitudinal and regional patterns in continental and suboceanic heath vegetation of northern Fennoscandia. Acta Bot Fenn 153:1–80.
Oksanen T, Oksanen L, Olofsson J. 2008. Arctic lemmings, Lemmus spp. and Dicrostonyx spp.: integrating ecological and evolutionary perspectives. Evol Ecol Res 10:415–34.
Oksanen T, Oksanen L, Söderbacka G, Hoset KS, Ruffino L, Tuomi M. 2013. Impact of marine-subsidized predators on lemming-plant oscillations: a case of predator-prey mutualism? Evol Ecol Res 15:1–24.
Olofsson J. 2006. Short- and long-term effects of changes in reindeer grazing pressure on tundra heath vegetation. J Ecol 94:431–40.
Olofsson J, Hulme PE, Oksanen L, Suominen O. 2004a. Importance of large and small mammalian herbivores for the plant community structure in the forest tundra ecotone. Oikos 106:324–34.
Olofsson J, Moen J, Oksanen L. 2002. Effects of herbivory on competition intensity in two arctic-alpine tundra communities with different productivity. Oikos 96:265–72.
Olofsson J, Oksanen L, Callaghan T, Hulme PE, Oksanen T, Suominen O. 2009. Herbivores inhibit climate-driven shrub expansion on the tundra. Glob Chang Biol 15:2681–93.
Olofsson J, Stark S, Oksanen L. 2004b. Reindeer influence on ecosystem processes in the tundra. Oikos 105:386–96.
Olofsson J, Tømmervik H, Callaghan TV. 2012. Vole and lemming activity observed from space. Nat Clim Chang 2:880–3.
Pastor J, Dewey B, Naiman RJ, McInnes PF, Cohen Y. 1993. Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–80.
Pastor J, Naiman RJ. 1992. Selective foraging and ecosystem processes in boreal forests. Am Nat 139:690–705.
Polis GA, Sears ALW, Huxel GR, Strong DR, Maron J. 2000. When is a trophic cascade a trophic cascade? Trends Ecol Evol 15:473–5.
Polis GA, Strong DR. 1996. Food web complexity and community dynamics. Am Nat 147:813–46.
R Development Core Team. 2008. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org.
Ravolainen VT, Bråthen KA, Ims RA, Yoccoz NG, Henden JA, Killengreen ST. 2011. Rapid, landscape scale responses in riparian tundra vegetation to exclusion of small and large mammalian herbivores. Basic Appl Ecol 12:643–53.
Ripple WJ, Beschta RL. 2012. Large predators limit herbivore densities in northern forest ecosystems. Eur J Wildl Res 58:733–42.
Ripple WJ, Rooney TP, Beschta RL. 2010. Large predators, deer, and trophic cascades in the mid-latitudes. In: Terborgh J, Estes JA, Eds. Trophic cascades: predators, prey, and the changing dynamics of nature. Washington, DC: Island Press. p 141–61.
Strong DR. 1992. Are trophic cascades all wet? Differentiation and donor-control in speciose ecosystems. Ecology 73:747–54.
Terborgh J, Feeley K. 2010. Propagation of trophic cascades via multiple pathways in tropical forests. In: Terborgh J, Estes JA, Eds. Trophic cascades: predators, prey, and the changing dynamics of nature. Washington, DC: Island Press. p 125–40.
Tilman D. 1988. Plant strategies and the dynamics and structure of plant communities. Princeton: Princeton University Press.
Virtanen R. 1998. Impact of grazing and neighbour removal on a heath plant community transplanted onto a snowbed site, NW Finnish Lapland. Oikos 81:359–67.
Virtanen R. 2000. Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland. Oikos 90:295–300.
Virtanen R, Parviainen J, Henttonen H. 2002. Winter grazing by the Norwegian lemming (Lemmus lemmus) at Kilpisjarvi (NW Finnish Lapland) during a moderate population peak. Ann Zool Fenn 39:335–41.
Virtanen RJ, Lundberg PA, Moen J, Oksanen L. 1997. Topographic and altitudinal patterns in plant communities on European arctic islands. Polar Biol 17:95–113.
Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Elvebakk A, Gould WA, Katenin AE, Kholod SS, Markon CJ, Melnikov ES, Moskalenko NG, Talbot SS, Yurtsev BA, Team C. 2005. The circumpolar arctic vegetation map. J Veg Sci 16:267–82.
Zimov SA, Chuprynin VI, Oreshko AP, Chapin FS, Reynolds JF, Chapin MC. 1995. Steppe-tundra transition: a herbivore-driven biome shift at the end of the Pleistocene. Am Nat 146:765–94.
Acknowledgments
This study would not have been possible without the help of our devoted field assistants. The author especially thank Mirjam Szwierczynski and Karolina Norrman for their work. The logistic services provided by Steinar Kristensen at Joatka tundra lodge were crucial for our success. The study was supported by the Swedish Research Council, the Academy of Finland, and internal grants from the University of Turku and Finnmark University College. The team belongs to the Nordic Centre of Excellence TUNDRA, funded by the Norden Top-Level Research Initiative “Effect Studies and Adaptation to Climate Change.”
Author information
Authors and Affiliations
Corresponding author
Additional information
Author Contributions
All coauthors contributed to the fieldwork. LO and JO designed the study, analyzed the data and wrote the paper with substantial contributions from all the other coauthors.
Rights and permissions
About this article
Cite this article
Olofsson, J., Oksanen, L., Oksanen, T. et al. Long-Term Experiments Reveal Strong Interactions Between Lemmings and Plants in the Fennoscandian Highland Tundra. Ecosystems 17, 606–615 (2014). https://doi.org/10.1007/s10021-013-9740-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10021-013-9740-6