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Ecosystems

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Muskoxen Modify Plant Abundance, Phenology, and Nitrogen Dynamics in a High Arctic Fen

  • Jesper Bruun MosbacherEmail author
  • Anders Michelsen
  • Mikkel Stelvig
  • Håvard Hjermstad-Sollerud
  • Niels Martin Schmidt
Article

Abstract

Herbivores are key drivers of vegetation dynamics in most ecosystems. However, the effect of high arctic herbivores on vegetation dynamics throughout a growing season is not well understood. In this study, we examine the impacts of a large dominant herbivore in the tundra ecosystem, the muskox, Ovibos moschatus, using exclosures established in a fen in high Arctic Greenland. Using weekly sampling throughout the growing season, we quantified the effects of muskox exclusion on aboveground plant biomass and on concentrations and pools of carbon and nitrogen, and explored the timing of peak biomass and nutrient pools. Excluding muskoxen profoundly changed plant abundances and dynamics of the fen, with more than a doubling of aboveground plant biomass and carbon and nitrogen pool sizes. Specifically, large increases in mosses and litter were observed, while graminoid biomass did not change significantly with exclusion of muskoxen. Excluding muskoxen advanced the peak of plant biomass, but also led to a more rapid decline, resulting in an earlier and shorter period of maximal plant biomass inside the exclosures. The largest impact of muskoxen on the arctic fen ecosystem seems to be through their trampling effects on the moss layer, which likely mediated most of the observed changes. This study demonstrates how quickly an ecosystem may respond to changes in the abundance of large herbivores and highlights their pivotal role in modifying vegetation dynamics and nutrient cycling in tundra ecosystems.

Keywords

biomass exclosures grazing herbivore nitrogen pools Ovibos moschatus trampling tundra Zackenberg 

Notes

Acknowledgements

Aarhus University is thanked for providing access to the Zackenberg Research Station. We are grateful for the financial support from 15. Juni Fonden, Arctic Research Centre at Aarhus University, and the Danish National Research Foundation for supporting CENPERM (DNRF 100). Special thanks are due to Lars Holst Hansen, Jannik Hansen, and Christian Bay for their assistance in the field, and to Gosha Sylvester for assistance in the laboratory.

Supplementary material

10021_2018_323_MOESM1_ESM.pdf (28 kb)
Supplementary material 1 (PDF 29 kb)
10021_2018_323_MOESM2_ESM.pdf (7 kb)
Supplementary material 2 (PDF 8 kb)
10021_2018_323_MOESM3_ESM.docx (16 kb)
Supplementary material 3 (DOCX 16 kb)

References

  1. Arndal MF, Illeris L, Michelsen A, Albert K, Tamstorf M, Hansen BU. 2009. Seasonal variation in gross ecosystem production, plant biomass, and carbon and nitrogen pools in five high Arctic vegetation types. Arct Antarct Alp Res 41:164–73.CrossRefGoogle Scholar
  2. Bardgett RD, van der Wal R, Jónsdóttir IS, Quirk H, Dutton S. 2007. Temporal variability in plant and soil nitrogen pools in a high-Arctic ecosystem. Soil Biol Biochem 39:2129–37.CrossRefGoogle Scholar
  3. Barthelemy H, Stark S, Olofsson J. 2015. Strong responses of sub-Arctic plant communities to long-term reindeer feces manipulation. Ecosystems 18:740–51.CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48.CrossRefGoogle Scholar
  5. Bay C. 1998. Vegetation mapping of Zackenberg Valley, Northeast Greenland. Denmark: Danish Polar Center & Botanical Museum, University of Copenhagen.Google Scholar
  6. Bliss LC. 1986. Arctic ecosystems: their structure, function and herbivore carrying capacity. In: Gudmundsson O, Ed. Grazing research at northern latitudes: NATO ASI Series. New York: Springer. pp 5–25.CrossRefGoogle Scholar
  7. Bueno CG, Williamson SN, Barrio IC, Helgadóttir Á, HiK DS. 2016. Moss mediates the influence of shrub species on soil properties and processes in Alpine Tundra. PLoS ONE 11:e0164143.CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD. 2007. Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–65.CrossRefPubMedGoogle Scholar
  9. Doiron M, Gauthier G, Lévesque E. 2014. Effects of experimental warming on nitrogen concentration and biomass of forage plants for an Arctic herbivore. J Ecol 102:508–17.CrossRefGoogle Scholar
  10. Elberling B, Tamstorf MP, Michelsen A, Arndal MF, Sigsgaard C, Illeris L, Bay C, Hansen BU, Christensen TR, Hansen ES, Jakobsen BH, Beyens L. 2008. Soil and plant community-characteristics and dynamics at Zackenberg. Adv Ecol Res 40(40):223–48.CrossRefGoogle Scholar
  11. Elliott TL, Henry GHR. 2011. Effects of simulated grazing in ungrazed wet Sedge Tundra in the high Arctic. Arct Antarct Alp Res 43:198–206.CrossRefGoogle Scholar
  12. Elmendorf SC, Henry GHR, Hollister RD, Björk RG, Boulanger-Lapointe N, Cooper EJ, Cornelissen JHC, Day TA, Dorrepaal E, Elumveeva TG, Gill M, Gould WA, Harte J, Hik DS, Hofgaard A, Johnson DR, Johnstone JF, Jónsdóttir IS, Jorgensen JC, Klanderud K, Klein JA, Koh S, Kudo G, Lara M, Lévesque E, Magnusson B, May JL, Mercado-Diaz JA, Michelsen A, Molau U, Myers-Smith IH, Oberbauer SF, Onipchenko VG, Rixen C, Schmidt NM, Shaver G, Spasojevic MJ, Porhallsdóttir PE, Tolvanen A, Troxler T, Tweedie CE, Villareal S, Wahren C, Walker X, Webber PJ, Welker JM, Wipf S. 2012. Plot-scale evidence of tundra vegetation change and links to recent summer warming. Nat Clim Chang . 10.1038/nclimate1465.CrossRefGoogle Scholar
  13. Facelli J, Pickett SA. 1991. Plant litter: its dynamics and effects on plant community structure. Bot Rev 57:1–32.CrossRefGoogle Scholar
  14. Falk JM, Schmidt NM, Christensen TR, Ström L. 2015. Large herbivore grazing affects the vegetation structure and greenhouse gas balance in a high Arctic mire. Environ Res Lett 10:045001.CrossRefGoogle Scholar
  15. Falk JM, Schmidt NM, Ström L. 2014. Effects of simulated increased grazing on carbon allocation patterns in a high Arctic mire. Biogeochemistry 119:229–44.CrossRefGoogle Scholar
  16. Forchhammer MC, Post E, Berg TBG, Høye TT, Schmidt NM. 2005. Local-scale and short-term herbivore-plant spacial dynamics reflect influences of a large-scale climate. Ecology 86:2644–51.CrossRefGoogle Scholar
  17. Gornall J, Woodin S, Jónsdóttir I, Van der Wal R. 2009. Herbivore impacts to the moss layer determine tundra ecosystem response to grazing and warming. Oecologia 161:747–58.CrossRefPubMedGoogle Scholar
  18. Gornall JL, Jónsdóttir IS, Woodin SJ, Van der Wal R. 2007. Arctic mosses govern below-ground environment and ecosystem processes. Oecologia 153:931–41.CrossRefPubMedGoogle Scholar
  19. Gornall JL, Woodin SJ, Jónsdóttir IS, van der Wal R. 2011. Balancing positive and negative plant interactions: how mosses structure vascular plant communities. Oecologia 166:769–82.CrossRefPubMedGoogle Scholar
  20. Gough L, Shrestha K, Johnson DR, Moon B. 2008. Long-term mammalian herbivory and nutrient addition alter lichen community structure in Alaskan dry heath Tundra. Arct Antarct Alp Res 40:65–73.CrossRefGoogle Scholar
  21. Hansen BU, Sigsgaard C, Rasmussen L, Cappelen J, Hinkler J, Mernild SH, Petersen D, Tamstorf MP, Rasch M, Hasholt B. 2008. Present-day climate at Zackenberg. Adv Ecol Res 40(40):111–49.CrossRefGoogle Scholar
  22. Henry GHR, Svoboda J, Freedman B. 1990. Standing crop and net production of sedge meadows of an ungrazed polar desert oasis. Can J Bot 68:2660–7.CrossRefGoogle Scholar
  23. Hobara S, McCalley C, Koba K, Giblin AE, Weiss MS, Gettel GM, Shaver GR. 2006. Nitrogen fixation in surface soils and vegetation in an Arctic Tundra watershed: a key source of atmospheric nitrogen. Arct Antarct Alp Res 38:363–72.CrossRefGoogle Scholar
  24. Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biom J 50:346–63.CrossRefPubMedGoogle Scholar
  25. Høye TT, Post E, Meltofte H, Schmidt NM, Forchhammer MC. 2007. Rapid advancement of spring in the high Arctic. Curr Biol 17:R449–51.CrossRefPubMedGoogle Scholar
  26. Ihl C, Barboza PS. 2007. Nutritional value of moss for Arctic ruminants: a test with muskoxen. J Wildl Manage 71:752–8.CrossRefGoogle Scholar
  27. Jefferies RL, Klein CJ, Shaver G. 1994. Vertebrate herbivores and northern plant communities: reciprocal influences and responses. Oikos 71:193–206.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. Kaarlejärvi E, Hoset KS, Olofsson J. 2015. Mammalian herbivores confer resilience of Arctic shrub-dominated ecosystems to changing climate. Glob Chang Biol 21:3379–88.CrossRefPubMedGoogle Scholar
  30. Kristensen DK, Kristensen E, Forchhammer MC, Michelsen A, Schmidt NM. 2011. Arctic herbivore diet can be inferred from stable carbon and nitrogen isotopes in C3 plants, faeces, and wool. Can J Zool 89:893–900.CrossRefGoogle Scholar
  31. Kuznetsova A, Brockhoff PB, Christensen RHB. 2016. lmerTest: tests in linear mixed effects models. R package version 2.0-33. http://CRAN.R-project.org/package=lmerTest.
  32. Lepage D, Gauthier G, Reed A. 1998. Seasonal variation in growth of greater snow goose goslings: the role of food supply. Oecologia 114:226–35.CrossRefPubMedGoogle Scholar
  33. Lett S, Michelsen A. 2014. Seasonal variation in nitrogen fixation and effects of climate change in a sub-Arctic heath. Plant Soil 379:193–204.CrossRefGoogle Scholar
  34. Maron JL, Crone E. 2006. Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc B Biol Sci 273:2575–84.CrossRefGoogle Scholar
  35. Mosbacher JB, Kristensen DK, Michelsen A, Stelvig M, Schmidt NM. 2016a. Quantifying muskox biomass removal and spatial relocation of nitrogen in a high Arctic Tundra ecosystem. Arct Antarct Alp Res 48:229–40.CrossRefGoogle Scholar
  36. Mosbacher JB, Michelsen A, Stelvig M, Hendrichsen DK, Schmidt NM. 2016b. Show me your rump hair and I will tell you what you ate—The dietary history of Muskoxen (Ovibos moschatus) revealed by sequential stable isotope analysis of guard hairs. PLoS ONE 11:e0152874.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mulder CPH. 1999. Vertebrate herbivores and plants in the Arctic and sub-Arctic: effects on individuals, populations, communities and ecosystems. Perspect Plant Ecol Evol Syst 2:29–55.CrossRefGoogle Scholar
  38. Murray JL. 1991. Biomass distribution and nutrient pool and dynamics in the major muskox-grazed communities at Sverdup Pass (79 N), Ellesmere Island, N.W.T., Canada. Canada: University of Toronto. pp 1–183.Google Scholar
  39. Myers-Smith IH, Elmendorf SC, Beck PSA, Wilmking M, Hallinger M, Blok D, Tape KD, Rayback SA, Macias-Fauria M, Forbes BC, Speed JDM, Boulanger-Lapointe N, Rixen C, Levesque E, Schmidt NM, Baittinger C, Trant AJ, Hermanutz L, Collier LS, Dawes MA, Lantz TC, Weijers S, Jorgensen RH, Buchwal A, Buras A, Naito AT, Ravolainen V, Schaepman-Strub G, Wheeler JA, Wipf S, Guay KC, Hik DS, Vellend M. 2015. Climate sensitivity of shrub growth across the tundra biome. Nat Clim Chang 5:887–91.CrossRefGoogle Scholar
  40. Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA. 1991. Effects of temperature and substrate quality on element mineralization in 6 Arctic soils. Ecology 72:242–53.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. Olofsson J, Stark S, Oksanen L. 2004. Reindeer influence on ecosystem processes in the tundra. Oikos 105:386.CrossRefGoogle Scholar
  44. Piedboeuf N, Gauthier G. 1999. Nutritive quality of forage plants for greater snow goose goslings: When is it advantageous to feed on grazed plants? Can J Zool 77:1908–18.CrossRefGoogle Scholar
  45. Post E. 2013. Erosion of community diversity and stability by herbivore removal under warming. Proc R Soc B Biol Sci 280.CrossRefPubMedGoogle Scholar
  46. Post E, Bøving PS, Pedersen C, MacArthur MA. 2003. Synchrony between caribou calving and plant phenology in depredated and non-depredated populations. Can J Zool 81:1709–14.CrossRefGoogle Scholar
  47. Post E, Forchhammer MC. 2008. Climate change reduces reproductive success of an Arctic herbivore through trophic mismatch. Philos Trans R Soc B Biol Sci 363:2369–75.CrossRefGoogle Scholar
  48. Post E, Pedersen C. 2008. Opposing plant community responses to warming with and without herbivores. Proc Natl Acad Sci 105:12353–8.CrossRefPubMedGoogle Scholar
  49. Post E, Pedersen C, Wilmers CC, Forchhammer MC. 2008. Warming, plant phenology and the spatial dimension of trophic mismatch for large herbivores. Proc R Soc B Biol Sci 275:2005–13.CrossRefGoogle Scholar
  50. Price PW. 2002. Resource-driven terrestrial interaction webs. Ecol Res 17:241–7.CrossRefGoogle Scholar
  51. R Core Team (2015). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
  52. Raillard M, Svoboda J. 2000. High grazing impact, selectivity, and local density of muskoxen in central Ellesmere Island, Canadian high Arctic. Arct Antarct Alp Res 32:278–85.CrossRefGoogle Scholar
  53. Ravolainen VT, Bråthen KA, Yoccoz NG, Nguyen JK, Ims RA. 2014. Complementary impacts of small rodents and semi-domesticated ungulates limit tall shrub expansion in the tundra. J Appl Ecol 51:234–41.CrossRefGoogle Scholar
  54. Rinnan R, Stark S, Tolvanen A. 2009. Responses of vegetation and soil microbial communities to warming and simulated herbivory in a sub-Arctic heath. J Ecol 97:788–800.CrossRefGoogle Scholar
  55. Rousk K, Sørensen PL, Michelsen A. 2017. Nitrogen fixation in the High Arctic: a source of ‘new’ nitrogen? Biogeochemistry 136:213–22.CrossRefGoogle Scholar
  56. Schmidt NM, Beest FMV, Mosbacher JB, Stelvig M, Hansen LH, Nabe-Nielsen J, Grøndahl C. 2016. Ungulate movement in an extreme seasonal environment: year-round movement patterns of high-Arctic muskoxen. Wildl Biol 22:253–67.CrossRefGoogle Scholar
  57. Schmidt NM, Kristensen DK, Michelsen A, Bay C. 2012. High Arctic plant community responses to a decade of ambient warming. Biodiversity 13:191–9.CrossRefGoogle Scholar
  58. Schmidt NM, Krogh PH, Forchhammer MC. 2011. Herbivore influences on ecosystem functioning: establishment of musk ox exclosures at Zackenberg. Technical report from DCE—Danish Centre for Environment and Energy: Aarhus University, Department of Bioscience.Google Scholar
  59. Schmidt NM, Pedersen SH, Mosbacher JB, Hansen LH. 2015. Long-term patterns of muskox (Ovibos moschatus) demographics in high Arctic Greenland. Polar Biol 38:1667–75.CrossRefGoogle Scholar
  60. Shaver GR, Chapin FS. 1991. Production: biomass relationships and element cycling in contrasting Arctic vegetation types. Ecol Monogr 61:1–31.CrossRefGoogle Scholar
  61. Sjögersten S, van der Wal R, Woodin SJ. 2012. Impacts of grazing and climate warming on C pools and decomposition rates in Arctic environments. Ecosystems 15:349–62.CrossRefGoogle Scholar
  62. Sørensen LI, Mikola J, Kytöviita M-M, Olofsson J. 2009. Trampling and spatial heterogeneity explain decomposer abundances in a sub-Arctic grassland subjected to simulated reindeer grazing. Ecosystems 12:830–42.CrossRefGoogle Scholar
  63. Stark S, Grellmann D. 2002. Soil microbial responses to herbivory in an Arctic Tundra heath at two levels of nutrient availability. Ecology 83:2736–44.CrossRefGoogle Scholar
  64. Ström L, Tagesson T, Mastepanov M, Christensen TR. 2012. Presence of Eriophorum scheuchzeri enhances substrate availability and methane emission in an Arctic wetland. Soil Biol Biochem 45:61–70.CrossRefGoogle Scholar
  65. Thackeray SJ, Henrys PA, Hemming D, Bell JR, Botham MS, Burthe S, Helaouet P, Johns DG, Jones ID, Leech DI, Mackay EB, Massimino D, Atkinson S, Bacon PJ, Brereton TM, Carvalho L, Clutton-Brock TH, Duck C, Edwards M, Elliott JM, Hall SJG, Harrington R, Pearce-Higgins JW, Høye TT, Kruuk LEB, Pemberton JM, Sparks TH, Thompson PM, White I, Winfield IJ, Wanless S. 2016. Phenological sensitivity to climate across taxa and trophic levels. Nature 535:241–5.CrossRefPubMedGoogle Scholar
  66. Van Beest FM, Mysterud A, Loe LE, Milner JM. 2010. Forage quantity, quality and depletion as scale-dependent mechanisms driving habitat selection of a large browsing herbivore. J Anim Ecol 79:910–22.PubMedGoogle Scholar
  67. Van der Putten WH, Macel M, Visser ME. 2010. Predicting species distribution and abundance responses to climate change: why it is essential to include biotic interactions across trophic levels. Philos Trans R Soc Lond B Biol Sci 365:2025–34.CrossRefPubMedPubMedCentralGoogle Scholar
  68. van der Wal R. 2006. Do herbivores cause habitat degradation or vegetation state transition? Evidence from the Tundra. Oikos 114:177–86.CrossRefGoogle Scholar
  69. van der Wal R, Bardgett RD, Harrison KA, Stien A. 2004. Vertebrate herbivores and ecosystem control: cascading effects of faeces on Tundra ecosystems. Ecography 27:242–52.CrossRefGoogle Scholar
  70. van der Wal R, Brooker RW. 2004. Mosses mediate grazer impacts on grass abundance in Arctic ecosystems. Funct Ecol 18:77–86.CrossRefGoogle Scholar
  71. van der Wal R, Hessen DO. 2009. Analogous aquatic and terrestrial food webs in the high Arctic: the structuring force of a harsh climate. Perspect Plant Ecol Evol Syst 11:231–40.CrossRefGoogle Scholar
  72. van der Wal R, Madan N, van Lieshout S, Dormann C, Langvatn R, Albon SD. 2000. Trading forage quality for quantity? Plant phenology and patch choice by Svalbard reindeer. Oecologia 123:108–15.CrossRefPubMedGoogle Scholar
  73. van der Wal RR, van Lieshout SMJ, Loonen MJJE. 2001. Herbivore impact on moss depth, soil temperature and Arctic plant growth. 24:29–32.Google Scholar
  74. Westergaard-Nielsen A, Lund M, Pedersen SH, Schmidt NM, Klosterman S, Abermann J, Hansen BU. 2017. Transitions in high-Arctic vegetation growth patterns and ecosystem productivity tracked with automated cameras from 2000 to 2013. Ambio 46:39–52.CrossRefPubMedPubMedCentralGoogle Scholar
  75. White TC. 2012. The inadequate environment: nitrogen and the abundance of animals. Springer.Google Scholar
  76. Ylänne H, Stark S, Tolvanen A. 2015. Vegetation shift from deciduous to evergreen dwarf shrubs in response to selective herbivory offsets carbon losses: evidence from 19 years of warming and simulated herbivory in the sub-Arctic Tundra. Glob Chang Biol 21:3696–711.CrossRefPubMedGoogle Scholar
  77. Zamin TJ, Grogan P. 2013. Caribou exclusion during a population low increases deciduous and evergreen shrub species biomass and nitrogen pools in low Arctic Tundra. J Ecol 101:671–83.CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Arctic Research Centre, Department of BioscienceAarhus UniversityRoskildeDenmark
  2. 2.Department of BiologyUniversity of CopenhagenCopenhagen ØDenmark
  3. 3.Center for Permafrost, University of CopenhagenCopenhagen KDenmark
  4. 4.Copenhagen ZooFrederiksbergDenmark

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