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

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.

This is a preview of subscription content, log in to check access.

Figure 1
Figure 2
Figure 3
Figure 4

References

  1. Adhikari K, Hartemink AE. 2016. Linking soils to ecosystem services—a global review. Geoderma 262:101–11.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  6. Bardgett RD, Wardle DA. 2003. Herbivore-mediated linkages between aboveground and belowground communities. Ecology 84:2258–68.

    Article  Google 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.

    Article  PubMed  Google 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.

    Article  Google Scholar 

  9. Blum WEH. 2005. Functions of soil for society and the environment. Rev Environ Sci Bio/Technol 4:75–9.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  12. Davidson DW. 1993. The effects of herbivory and granivory on terrestrial plant succession. Oikos 68:23–35.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

  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.

    Article  CAS  Google 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.

    Article  PubMed  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  25. Kielland K, Bryant JP. 1998. Moose herbivory in taiga: effects on biogeochemistry and vegetation dynamics in primary succession. Oikos 82:377–83.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  29. Kuznetsova A, Brockhoff PB, Bojesen RH. 2016. lmerTest: tests in linear mixed effects models. R package version 2.0-33.

  30. Kuzyakov Y, Friedel J, Stahr K. 2000. Review of mechanisms and quantification of priming effects. Soil Biol Biochem 32:1485–98.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

  35. Muller RN. 1978. The phenology, growth and ecosystem dynamics of Erythronium americanum in the northern hardwood forest. Ecol Monogr 48:1–20.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

  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.

    Article  CAS  Google 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.

    Article  Google Scholar 

  41. Pastor J, Naiman RJ. 1992. Selective foraging and ecosystem processes in boreal forests. Am Nat 139:690–705.

    Article  Google Scholar 

  42. Patzel N, Sticher H, Karlen DL. 2000. Soil fertility-phenomenon and concept. J Plant Nutr Soil Sci 163:129–42.

    Article  CAS  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

    Article  Google 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.

    Article  CAS  Google 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.

    Article  Google Scholar 

  56. Tamm CO. 1991. Nitrogen in terrestrial ecosystems: questions of productivity, vegetational changes, and ecosystem stability. Berlin: Springer.

    Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  PubMed  CAS  Google 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.

    Article  Google 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.

    Article  PubMed  CAS  Google 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.

    Article  Google 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.

    Article  Google 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.

    Article  Google Scholar 

Download references

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.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Anders Lorentzen Kolstad.

Additional information

Author contributions

The study was planned by ALK, GA, EJS, SJW and JDMS. Field work was conducted by ALK, GA, AMAV and JDMS. Laboratory work was conducted by ALK and AMAV. Statistical analyses were conducted by ALK, with a significant input from JDMS. ALK wrote the manuscript with input from all co-authors.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 2005 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kolstad, A.L., Austrheim, G., Solberg, E.J. et al. Cervid Exclusion Alters Boreal Forest Properties with Little Cascading Impacts on Soils. Ecosystems 21, 1027–1041 (2018). https://doi.org/10.1007/s10021-017-0202-4

Download citation

Keywords

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