Abstract
Deposition of feces is a key mechanism by which herbivores influence soil nutrient cycling and plant production, but the knowledge about its importance for plant production and community structure is still rudimental since experimental evidence is scarce. We thus performed a 7-year long reindeer feces manipulation experiment in two tundra vegetation types with contrasting nutrient availability and analyzed effects on plant community composition and soil nutrient availability. Despite feces being fairly nutrient poor, feces manipulation had strong effect on both the nutrient-poor heath and the nutrient-rich meadow. The strongest effect was detected when feces were added at high density, with a substantial increase in total vascular plant productivity and graminoids in the two communities. Doubling natural deposition of reindeer feces enhanced primary production and the growth of deciduous shrubs in the heath. By contrast, removal of feces decreased only the production of graminoids and deciduous shrubs in the heath. Although the response to feces addition was faster in the nutrient-rich meadow, after 7 years it was more pronounced in the nutrient-poor heath. The effect of feces manipulation on soil nutrient availability was low and temporarily variable. Our study provides experimental evidence for a central role of herbivore feces in regulating primary production when herbivores are abundant enough. Deposition of feces alone does, however, not cause dramatic vegetation shifts; to drive unproductive heath to a productive grass dominated state, herbivore trampling, and grazing are probably also needed.
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References
Aerts R, Chapin FS. 2000. The mineral nutrition of wild plants revisited: a re-evaluation of processes and patterns. Adv Ecol Res 30:1–67.
Augustine DJ, McNaughton SJ, Frank DA. 2003. Feedbacks between soil nutrients and large herbivores in a managed savanna ecosystem. Ecol Appl 13:1325–37.
Bakker ES, Knops JMH, Milchunas DG, Ritchie ME, Olff H. 2009. Cross-site comparison of herbivore impact on nitrogen availability in grasslands: the role of plant nitrogen concentration. Oikos 118:1613–22.
Bardgett RD, Jones AC, Jones DL, Kemmitt SJ, Cook R, Hobbs PJ. 2001. Soil microbial community patterns related to the history and intensity of grazing in sub-montane ecosystems. Soil Biol Biochem 33:1653–64.
Bardgett RD, Wardle DA. 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–68.
Bazely DR, Jefferies RL. 1985. Goose feces—a source of nitrogen for plant-growth in a grazed salt-marsh. J Appl Ecol 22:693–703.
Blakemore LC, Daly BK, Searly PL. 1987. Methods for chemical analysis of soils. New Zealand Soil Bureau Scientific Report 80: Department of Scientific and Industrial Research, Wellington, New Zealand.
Bret-Harte MS, Mack MC, Goldsmith GR, Sloan DB, DeMarco J, Shaver GR, Ray PM, Biesinger Z, Chapin FS. 2008. Plant functional types do not predict biomass responses to removal and fertilization in Alaskan tussock tundra. J Ecol 96:713–26.
Brookes PC, Landman A, Pruden G, Jenkinson DS. 1985. Chloroform fumigation and the release of soil nitrogen—a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–42.
Chapin FS, Shaver GR. 1996. Physiological and growth responses of arctic plants to a field experiment simulating climatic change. Ecology 77:822–40.
Chapin FS, Shaver GR, Giblin AE, Nadelhoffer KJ, Laundre JA. 1995. Responses of arctic tundra to experimental and observed changes in climate. Ecology 76:694–711.
Cherif M, Loreau M. 2013. Plant-herbivore-decomposer stoichiometric mismatches and nutrient cycling in ecosystems. Proc R Soc B 280:20122453.
Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N, Quested HM, Santiago LS, Wardle DA, Wright IJ, Aerts R, Allison SD, van Bodegom P, Brovkin V, Chatain A, Callaghan TV, Diaz S, Garnier E, Gurvich DE, Kazakou E, Klein JA, Read J, Reich PB, Soudzilovskaia NA, Vaieretti MV, Westoby M. 2008. Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecol Lett 11:1065–71.
Day TA, Detling JK. 1990. Grassland patch dynamics and herbivore grazing preference following urine deposition. Ecology 71:180–8.
Eskelinen A. 2008. Herbivore and neighbour effects on tundra plants depend on species identity, nutrient availability and local environmental conditions. J Ecol 96:155–65.
Frank DA, Groffman PM. 1998. Ungulate vs. landscape control of soil C and N processes in grasslands of Yellowstone National Park. Ecology 79:2229–41.
Frank DA, Inouye RS, Huntly N, Minshall GW, Anderson JE. 1994. The biogeochemistry of a north-temperate grassland with native ungulates—nitrogen dynamics in Yellowstone National Park. Biogeochemistry 26:163–88.
Frank DA, McNaughton SJ. 1992. The ecology of plants, large mammalian herbivores, and drought in Yellowstone-National-Park. Ecology 73:2043–58.
Giesler R, Esberg C, Lagerstrom A, Graae BJ. 2012. Phosphorus availability 481 and microbial respiration across different tundra vegetation types. Biogeochemistry 108:429–45.
Gornall JL, Jonsdottir IS, Woodin SJ, Van der Wal R. 2007. Arctic mosses govern below ground environment and ecosystem processes. Oecologia 153:931–41.
Grellmann D. 2002. Plant responses to fertilization and exclusion of grazers on an arctic tundra heath. Oikos 98:190–204.
Hobbs NT. 1996. Modification of ecosystems by ungulates. J Wildl Manag 60:695–713.
Hodge A, Robinson D, Fitter A. 2000. Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–8.
Jonasson S. 1992. Plant-responses to fertilization and species removal in tundra related to community structure and clonality. Oikos 63:420–9.
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 80:1828–43.
Jonasson S, Michelsen A, Schmidt IK, Nielsen EV, Callaghan TV. 1996. Microbial biomass C, N and P in two arctic soils and responses to addition of NPK fertilizer and sugar: Implications for plant nutrient uptake. Oecologia 106:507–15.
Lindwall F, Vowles T, Ekblad A, Björk RG. 2013. Reindeer grazing has contrasting effect on species traits in Vaccinium vitis-idaea L. and Bistorta vivpara (L.) Gray. Acta Oecol 53:33–7.
McNaughton SJ. 1979. Grazing as an optimization process—grass ungulate relationships in the serengeti. Am Nat 113:691–703.
Michelsen A, Graglia E, Schmidt IK, Jonasson S, Sleep D, Quarmby C. 1999. Differential responses of grass and a dwarf shrub to long-term changes in soil microbial biomass C, N and P following factorial addition of NPK fertilizer, fungicide and labile carbon to a heath. New Phytol 143:523–38.
Murphy J, Riley JP. 1962. A modified single solution method for the determination of phosphate in natural-waters. Anal Chim Acta 27:31–6.
Olofsson J. 2004. Positive and negative plant-plant interactions in two contrasting alpine plant communities. Arct Antarct Alp Res 36:464–7.
Olofsson J. 2009. Effects of simulated reindeer grazing, trampling, and waste products on nitrogen mineralization and primary production. Arct Antarct Alp Res 41:330–8.
Olofsson J, Oksanen L. 2005. Effects of reindeer density on vascular plant diversity on North Scandinavian mountains. Rangifer 25:5–25.
Olofsson J, Kitti H, Rautiainen P, Stark S, Oksanen L. 2001. Effects of summer grazing by reindeer on composition of vegetation, productivity and nitrogen cycling. Ecography 24:13–24.
Olofsson J, Stark S, Oksanen L. 2004. Reindeer influence on ecosystem processes in the tundra. Oikos 105:386–96.
Olofsson J, de Mazancourt C, Crawley MJ. 2008. Spatial heterogeneity and plant species richness at different spatial scales under rabbit grazing. Oecologia 156:825–34.
Olofsson J, Tommervik H, Callaghan TV. 2012. Vole and lemming activity observed from space. Nat Clim Change 2:880–3.
Pastor J, Cohen YTH. 2006. The role of large herbivores in ecosystem nutrient cycles. In: Danell K, Bergström R, Duncan P, Pastor J, Eds. Large mammalian herbivores, ecosystem dynamics, and conservation. Cambridge, MA: Cambridge University Press.
Pastor J, Naiman RJ. 1992. Selective foraging and ecosystem processes in boreal forests. Am Nat 139:690–705.
Pastor J, Dewey B, Moen J, Mladenoff DJ, White M, Cohen J. 2006. Spatial patterns in the moose-forest-soil ecosystem on Isle Royal, Michigan, USA. Ecol Appl 8:411–24.
R Core Team. 2013. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.
Ritchie ME, Tilman D, Knops JMH. 1998. Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–77.
Ruess RW, Hik DS, Jefferies RL. 1989. The role of lesser snow geese as nitrogen processors in a sub-arctic salt-marsh. Oecologia 79:23–9.
Schmidt IK, Jonasson S, Shaver GR, Michelsen A, Nordin A. 2002. Mineralization and distribution of nutrients in plants and microbes in four arctic ecosystems: responses to warming. Plant Soil 242:93–106.
Schrama M, Veen GF, Bakker ES, Ruifrok JL, Bakker JP, Olff H. 2013. An integrated perspective to explain nitrogen mineralization in grazed ecosystems. Perspect Plant Ecol Evolut Syst 15:32–44.
Shaver GR, Chapin FS. 1995. Long-term responses to factorial, NPK fertilizer treatment by Alaskan wet and moist tundra sedge species. Ecography 18:259–75.
Sjögersten S, Kuijper DPJ, Wal R, Loonen MJJE, Huiskes AHL, Woodin SJ. 2010. Nitrogen transfer between herbivores and their forage species. Polar Biol 33:1195–203.
Skarin A. 2008. Decay rate of reindeer pellet-groups. Rangifer 28:47–52.
Skarin A, Danell O, Bergstrom R, Moen J. 2010. Reindeer movement patterns in alpine summer ranges. Polar Biol 33:1263–75.
Stark S, Kytoviita MM. 2006. Simulated grazer effects on microbial respiration in a subarctic meadow: Implications for nutrient competition between plants and soil microorganisms. Appl Soil Ecol 31:20–31.
Stark S, Männistö M, Eskelinen A. 2015. When do grazers accelerate or decelerate soil carbon and nitrogen cycling in tundra? A test of theory on grazing effects at contrasting levels of habitat fertility. Oikos. doi:10.1111/oik.01355.
Van Cleve K, Alexander V. 1981. Nitrogen cycling in tundra and boreal ecosystems. Ecol Bull 33:375–404.
van der Wal R, Bardgett RD, Harrison KA, Stien A. 2004. Vertebrate herbivores and ecosystem control: cascading effects of feces on tundra ecosystems. Ecography 27:242–52.
Van der Wal R, Brooker RW. 2004. Mosses mediate grazer impacts on grass abundance in arctic ecosystems. Funct Ecol 18:77–86.
van der Wal R, van Lieshout SMJ, Loonen M. 2001. Herbivore impact on moss depth, soil temperature and arctic plant growth. Polar Biol 24:29–32.
Warenberg K. 1982. Reindeer forage plants in the early grazing season: Growth and nutritional content in relation to climatic conditions. Acta Phytogeogr Suec 70:1–71.
Williams BL, Shand CA, Hill M, O´Hara C, Smith S, Young ME. 1995. A procedure for the simultaneous oxidation of total soluble N and P in extracts of fresh and fumigated soils and litters. Commun Soil Sci Plant Anal 26:91–106.
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
We would like to thank the people working at the Abisko Research Station for their logistic support, Sirkka Aakkonen for great help in soil and microbial analysis and numerous field workers for their devotion. This study was supported by the grants from Stiftelsen Oscar och Lili Lamns Minne, Formas 2012-230, and the Nordic Centre of Excellence TUNDRA, funded by the Norden Top-Level Research Initiative “Effect Studies and Adaptation to Climate Change”.
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JO and SS conceived and designed the study; JO, SS and HPL performed research and HPL analyzed the data and wrote the paper with comments from JO and SS.
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Barthelemy, H., Stark, S. & Olofsson, J. Strong Responses of Subarctic Plant Communities to Long-Term Reindeer Feces Manipulation. Ecosystems 18, 740–751 (2015). https://doi.org/10.1007/s10021-015-9856-y
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DOI: https://doi.org/10.1007/s10021-015-9856-y