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Ecosystems

, Volume 21, Issue 5, pp 1027–1041 | Cite as

Cervid Exclusion Alters Boreal Forest Properties with Little Cascading Impacts on Soils

  • Anders Lorentzen Kolstad
  • Gunnar Austrheim
  • Erling J. Solberg
  • Aurel M. A. Venete
  • Sarah J. Woodin
  • James D. M. Speed
Article
  • 333 Downloads

Abstract

Large herbivores are capable of modifying entire ecosystems with a combination of direct (for example browsing/grazing, trampling, defecation) and indirect (for example affecting plant species composition that then alters soil properties) effects. With many ungulate populations increasing across the northern hemisphere it is important to develop a general theory for how these animals can be expected to impact their habitats. Here we present the results of an 8-year experimental exclusion of moose (Alces alces) from 15 recent boreal forest clear-cut sites in Central Norway. We used standard univariate techniques to describe the treatment effect on multiple forest and soil properties and combined this with a multivariate Bayesian network structure learning approach to objectively assess the potential mechanistic pathways for indirect effects on soils and soil fertility. We found that excluding moose had predictable direct effects, such as increasing the ratio of deciduous to coniferous tree biomass and the canopy cover and decreasing soil bulk density and temperature. However, we found no treatment effects on any measures of soil processes or quality (decomposition, nitrogen availability, C/N ratio, pH, nutrient stocks), and furthermore, we found only limited evidence that the direct effects had cascading (indirect) effects on soils. These findings oppose the commonly held belief that moose exclusion will increase soil fertility, but still highlights the strong ability of moose to directly modify forested ecosystems.

Keywords

Alces alces cervid boreal forest herbivory Norway Bayesian network nitrogen availability tea bag index carbon stocks 

Notes

Acknowledgements

We wish to thank Marc Daverdin for helping with the fieldwork and with database management, Winta Berhie Gebreyohanis for helping with fieldwork and the calibration of the biomass models and Marte Fandrem for helping with fieldwork. Then we wish to thank the numerous landowners who let us use their forests for this long-term experiment. Finally, we are grateful to the two anonymous reviewers who gave insightful and critical feedback that helped us to improve this paper. The establishment of the experimental design and the field work was funded by the Research Council of Norway Environment 2015 programme (Project 184036), the Norwegian Environment Agency and Nord- and Sør-Trøndelag County Administration.

Supplementary material

10021_2017_202_MOESM1_ESM.docx (2 mb)
Supplementary material 1 (DOCX 2005 kb)

References

  1. Adhikari K, Hartemink AE. 2016. Linking soils to ecosystem services—a global review. Geoderma 262:101–11.CrossRefGoogle Scholar
  2. Andriuzzi WS, Wall DH. 2017. Responses of belowground communities to large aboveground herbivores: meta-analysis reveals biome-dependent patterns and critical research gaps. Glob Change Biol 23:3857–3869.CrossRefGoogle Scholar
  3. Apollonio M, Andersen R, Putman R. 2010. European ungulates and their management in the 21st century. Cambridge: Cambridge University Press.Google Scholar
  4. Austrheim G, Solberg EJ, Mysterud A. 2011. Spatio-temporal variation in large herbivore pressure in Norway during 1949–1999: has decreased grazing by livestock been countered by increased browsing by cervids? Wildl Biol 17:286–98.CrossRefGoogle Scholar
  5. Axelsson A-L, Östlund L. 2001. Retrospective gap analysis in a Swedish boreal forest landscape using historical data. For Ecol Manag 147:109–22.CrossRefGoogle Scholar
  6. Bardgett RD, Wardle DA. 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–68.CrossRefGoogle Scholar
  7. Beguin J, Pothier D, Côté SD. 2011. Deer browsing and soil disturbance induce cascading effects on plant communities: a multilevel path analysis. Ecol Appl 21:439–51.CrossRefPubMedGoogle Scholar
  8. Bjørneraas K, Solberg EJ, Herfindal I, Moorter BV, Rolandsen CM, Tremblay J-P, Skarpe C, Sæther B-E, Eriksen R, Astrup R. 2011. Moose Alces alces habitat use at multiple temporal scales in a human-altered landscape. Wildl Biol 17:44–54.CrossRefGoogle Scholar
  9. Blum WEH. 2005. Functions of soil for society and the environment. Rev Environ Sci Bio/Technol 4:75–9.CrossRefGoogle Scholar
  10. Cornelissen JH, Pérez-Harguindeguy N, Díaz S, Grime JP, Marzano B, Cabido M, Vendramini F, Cerabolini B. 1999. Leaf structure and defence control litter decomposition rate across species and life forms in regional floras on two continents. New Phytol 143:191–200.CrossRefGoogle Scholar
  11. Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM. 2004. Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–47.CrossRefGoogle Scholar
  12. Davidson DW. 1993. The effects of herbivory and granivory on terrestrial plant succession. Oikos 68:23–35.CrossRefGoogle Scholar
  13. Dominati E, Patterson M, Mackay A. 2010. A framework for classifying and quantifying the natural capital and ecosystem services of soils. Ecol Econ 69:1858–68.CrossRefGoogle Scholar
  14. Dufresne M, Bradley RL, Tremblay J-P, Poulin M, Pellerin S. 2009. Clearcutting and deer browsing intensity interact in controlling nitrification rates in forest floor. Ecoscience 16:361–8.CrossRefGoogle Scholar
  15. Edenius L, Bergman M, Ericsson G, Danell K. 2002. The role of moose as a disturbance factor in managed boreal forests. Silva Fennica 36:57–67.CrossRefGoogle Scholar
  16. Ellis NM, Leroux SJ. 2017. Moose directly slow plant regeneration but have limited indirect effects on soil stoichiometry and litter decomposition rates in disturbed maritime boreal forests. Funct Ecol 31:790–801.CrossRefGoogle Scholar
  17. Gass TM, Binkley D. 2011. Soil nutrient losses in an altered ecosystem are associated with native ungulate grazing. J Appl Ecol 48:952–60.CrossRefGoogle Scholar
  18. Granhus A, Hylen G, Nilsen J. 2012. Skogen i Norge: statistikk over skogforhold og skogressurser i Norge registrert i perioden 2005–2009. Ressursoversikt fra Skog og landskap 3: 12. Norwegian Forest and Landscape Institute, Ås, Norway.Google Scholar
  19. Harrison KA, Bardgett RD. 2004. Browsing by red deer negatively impacts on soil nitrogen availability in regenerating native forest. Soil Biol Biochem 36:115–26.CrossRefGoogle Scholar
  20. Hidding B, Tremblay J-P, Côté SD. 2013. A large herbivore triggers alternative successional trajectories in the boreal forest. Ecology 94:2852–60.CrossRefPubMedGoogle Scholar
  21. Huffman DW, Laughlin DC, Pearson KM, Pandey S. 2009. Effects of vertebrate herbivores and shrub characteristics on arthropod assemblages in a northern Arizona forest ecosystem. For Ecol Manag 258:616–25.CrossRefGoogle Scholar
  22. Hörnberg S. 2001. The relationship between moose (Alces alces) browsing utilisation and the occurrence of different forage species in Sweden. For Ecol Manag 149:91–102.CrossRefGoogle Scholar
  23. Kardol P, Dickie IA, John MGS, Husheer SW, Bonner KI, Bellingham PJ, Wardle DA. 2014. Soil-mediated effects of invasive ungulates on native tree seedlings. J Ecol 102:622–31.CrossRefGoogle Scholar
  24. Keuskamp JA, Dingemans BJJ, Lehtinen T, Sarneel JM, Hefting MM. 2013. Tea Bag Index: a novel approach to collect uniform decomposition data across ecosystems. Methods Ecol Evol 4:1070–5.CrossRefGoogle Scholar
  25. Kielland K, Bryant JP. 1998. Moose herbivory in taiga: effects on biogeochemistry and vegetation dynamics in primary succession. Oikos 82:377–83.CrossRefGoogle Scholar
  26. Kielland K, Bryant JP, Ruess RW. 1997. Moose herbivory and carbon turnover of early successional stands in interior Alaska. Oikos 80:25–30.CrossRefGoogle Scholar
  27. Kielland K, Bryant JP, Ruess RW. 2006a. Mammalian herbivory, ecosystem engineering, and ecological cascades in Alaskan boreal forests. In: Chapin FSIII, Oswood MW, Van Cleve K, Viereck LA, Verbyla DL, Eds. Alaska’s changing boreal forest. New York: Oxford University Press. p 211–26.Google Scholar
  28. Kielland K, Olson K, Ruess RW, Boone RD. 2006b. Contribution of winter processes to soil nitrogen flux in taiga forest ecosystems. Biogeochemistry 81:349–60.CrossRefGoogle Scholar
  29. Kuznetsova A, Brockhoff PB, Bojesen RH. 2016. lmerTest: tests in linear mixed effects models. R package version 2.0-33.Google Scholar
  30. Kuzyakov Y, Friedel J, Stahr K. 2000. Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–98.CrossRefGoogle Scholar
  31. Köster K, Berninger F, Köster E, Pumpanen J. 2015. Influences of reindeer grazing on above- and below-ground biomass and soil carbon dynamics. Arct Antarct Alp Res 47:495–503.CrossRefGoogle Scholar
  32. Laskurain NA, Aldezabal A, Olano JM, Loidi J, Escudero A. 2013. Intensification of domestic ungulate grazing delays secondary forest succession: evidence from exclosure plots. J Veg Sci 24:320–31.CrossRefGoogle Scholar
  33. Mathisen KM, Buhtz F, Danell K, Bergström R, Skarpe C, Suominen O, Persson IL. 2010. Moose density and habitat productivity affects reproduction, growth and species composition in field layer vegetation. J Veg Sci 21:705–16.Google Scholar
  34. McInnes PF, Naiman RJ, Pastor J, Cohen Y. 1992. Effects of moose browsing on vegetation and litter of the boreal forest, Isle Royale, Michigan, USA. Ecology 73:2059–75.CrossRefGoogle Scholar
  35. Muller RN. 1978. The phenology, growth and ecosystem dynamics of Erythronium americanum in the northern hardwood forest. Ecol Monogr 48:1–20.CrossRefGoogle Scholar
  36. Mysterud A, Yoccoz NG, Langvatn R, Pettorelli N, Stenseth NC. 2008. Hierarchical path analysis of deer responses to direct and indirect effects of climate in northern forest. Philos Trans R Soc Lond B Biol Sci 363:2357–66.CrossRefGoogle Scholar
  37. Månsson J, Kalén C, Kjellander P, Andrén H, Smith H. 2007. Quantitative estimates of tree species selectivity by moose (Alces alces) in a forest landscape. Scand J For Res 22:407–14.CrossRefGoogle Scholar
  38. Nagarajan R, Scutari M, Lèbre S. 2013. In: Bayesian Networks in R with Applications in Systems Biology. New York: Springer-Verlag. 157 p.Google Scholar
  39. Nasholm T, Ekblad A, Nordin A, Giesler R, Hogberg M, Hogberg P. 1998. Boreal forest plants take up organic nitrogen. Nature 392:914–16.CrossRefGoogle Scholar
  40. Pastor J, Dewey B, Naiman R, McInnes P, Cohen Y. 1993. Moose browsing and soil fertility in the boreal forests of Isle Royale National Park. Ecology 74:467–80.CrossRefGoogle Scholar
  41. Pastor J, Naiman RJ. 1992. Selective foraging and ecosystem processes in boreal forests. Am Nat 139:690–705.CrossRefGoogle Scholar
  42. Patzel N, Sticher H, Karlen DL. 2000. Soil fertility-phenomenon and concept. J Plant Nutr Soil Sci 163:129–42.CrossRefGoogle Scholar
  43. Persson I-L, Pastor J, Danell K, Bergström R. 2005. Impact of moose population density on the production and composition of litter in boreal forests. Oikos 108:297–306.CrossRefGoogle Scholar
  44. Prins HH, Gordon IJ. 2008. Introduction: grazers and browsers in a changing world. In: Gordon IJ, Prins HH, Eds. The ecology of browsing and grazing. Ecological studies, Vol. 195. Berlin: Springer. Google Scholar
  45. R Core Team. 2016. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.Google Scholar
  46. Relva MA, Castán E, Mazzarino MJ. 2014. Litter and soil properties are not altered by invasive deer browsing in forests of NW Patagonia. Acta Oecol 54:45–50.CrossRefGoogle Scholar
  47. Revelle W. 2016. Psych: procedures for personality and psychological research. V = 1.6.9. Evanston, IL: Northwestern University.Google Scholar
  48. Ritchie ME, Tilman D, Knops JM. 1998. Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165–77.CrossRefGoogle Scholar
  49. Solberg EJ, Rolandsen CM, Eriksen R, Astrup R. 2012. Fra Edens hage til vredens druer: Elgens beiterssurser i nord og i sør. Hjorteviltet 2012:22–8.Google Scholar
  50. Speed JD, Austrheim G, Hester AJ, Solberg EJ, Tremblay J-P. 2013. Regional-scale alteration of clear-cut forest regeneration caused by moose browsing. For Ecol Manag 289:289–99.CrossRefGoogle Scholar
  51. Speed JDM, Austrheim G, Hester AJ, Meisingset EL, Mysterud A, Tremblay JP, Øien DI, Solberg EJ. 2014. General and specific responses of understory vegetation to cervid herbivory across a range of boreal forests. Oikos 123:1270–80.CrossRefGoogle Scholar
  52. Stark S, Männistö MK, Smolander A. 2010. Multiple effects of reindeer grazing on the soil processes in nutrient-poor northern boreal forests. Soil Biol Biochem 42:2068–77.CrossRefGoogle Scholar
  53. Stark S, Wardle DA, Ohtonen R, Helle T, Yeates GW. 2000. The effect of reindeer grazing on decomposition, mineralization and soil biota in a dry oligotrophic Scots pine forest. Oikos 90:301–10.CrossRefGoogle Scholar
  54. Strand LT, Callesen I, Dalsgaard L, de Wit HA. 2016. Carbon and nitrogen stocks in Norwegian forest soils—the importance of soil formation, climate, and vegetation type for organic matter accumulation. Can J For Res 46:1459–73.CrossRefGoogle Scholar
  55. Sulkava P, Huhta V. 2003. Effects of hard frost and freeze-thaw cycles on decomposer communities and N mineralisation in boreal forest soil. Appl Soil Ecol 22:225–39.CrossRefGoogle Scholar
  56. Tamm CO. 1991. Nitrogen in terrestrial ecosystems: questions of productivity, vegetational changes, and ecosystem stability. Berlin: Springer.CrossRefGoogle Scholar
  57. Telfer ES. 1984. Circumpolar distribution and habitat requirements of moose (Alces alces). In: Gill D, Olson R, Hastings R, Geddes F, Eds. Northern ecology and resource management: memorial essays honouring Don Gill. Edmonton: University of Alberta Press. p 145–82.Google Scholar
  58. Tichý L. 2015. Field test of canopy cover estimation by hemispherical photographs taken with a smartphone. J Veg Sci 27:427–35.CrossRefGoogle Scholar
  59. Tremblay JP, Huot J, Potvin F. 2007. Density-related effects of deer browsing on the regeneration dynamics of boreal forests. J Appl Ecol 44:552–62.CrossRefGoogle Scholar
  60. Veen GF, Olff H, Duyts H, Van Der Putten WH. 2010. Vertebrate herbivores influence soil nematodes by modifying plant communities. Ecology 91:828–35.CrossRefPubMedGoogle Scholar
  61. Vesterdal L, Schmidt IK, Callesen I, Nilsson LO, Gundersen P. 2008. Carbon and nitrogen in forest floor and mineral soil under six common European tree species. For Ecol Manag 255:35–48.CrossRefGoogle Scholar
  62. Wardle DA, Bardgett RD, Klironomos JN, Setälä H, Van Der Putten WH, Wall DH. 2004. Ecological linkages between aboveground and belowground biota. Science 304:1629–33.CrossRefPubMedGoogle Scholar
  63. Wardle DA, Barker GM, Yeates GW, Bonner KI, Ghani A. 2001. Introduced browsing mammals in New Zealand natural forests: aboveground and belowground consequences. Ecol Monogr 71:587–614.CrossRefGoogle Scholar
  64. Yuste JC, Baldocchi DD, Gershenson A, Goldstein A, Misson L, Wong S. 2007. Microbial soil respiration and its dependency on carbon inputs, soil temperature and moisture. Glob Change Biol 13:2018–35.CrossRefGoogle Scholar
  65. Zhang D, Hui D, Luo Y, Zhou G. 2008. Rates of litter decomposition in terrestrial ecosystems: global patterns and controlling factors. J Plant Ecol 1:85–93.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2017

Authors and Affiliations

  • Anders Lorentzen Kolstad
    • 1
  • Gunnar Austrheim
    • 1
  • Erling J. Solberg
    • 2
  • Aurel M. A. Venete
    • 3
  • Sarah J. Woodin
    • 3
  • James D. M. Speed
    • 1
  1. 1.NTNU University MuseumNorwegian University of Science and TechnologyTrondheimNorway
  2. 2.Norwegian Institute for Nature ResearchTrondheimNorway
  3. 3.School of Biological SciencesUniversity of AberdeenAberdeenUK

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