Advertisement

Ecological Research

, Volume 31, Issue 6, pp 777–784 | Cite as

Red deer mediate spatial and temporal plant heterogeneity in boreal forests

  • Marte Synnøve Lilleeng
  • Stein Joar Hegland
  • Knut Rydgren
  • Stein R. Moe
Original Article

Abstract

Selective herbivory can influence both spatial and temporal vegetation heterogeneity. For example, many northern European populations of free-ranging ungulates have reached unprecedented levels, which can influence plant species turnover, long-term maintenance of biodiversity and the subsequent stability of boreal ecosystems. However, the mechanisms by which large herbivores affect spatial and temporal vegetation heterogeneity remain poorly understood. Here, we combined a 10-year exclusion experiment with a herbivore intensity gradient to investigate how red deer (Cervus elaphus) acts as a driver of temporal and spatial heterogeneity in the understory of a boreal forest. We measured the two dimensions of heterogeneity as temporal and spatial species turnover. We found that temporal heterogeneity was positively related to herbivory intensity, and we found a similar trend for spatial heterogeneity. Removing red deer (exclosure) from our study system caused a distinct shift in species composition, both spatially (slow response) and temporally (quick response). Vegetation from which red deer had been excluded for 10 years showed the highest spatial heterogeneity, suggesting that the most stable forest understory will occur where there are no large herbivores. However, excluding red deer resulted in lower species diversity and greater dominance by a low number of plant species. If both stable but species rich ecosystems are the management goal, these findings suggest that naturally fluctuating, but moderate red deer densities should be sustained.

Keywords

Biodiversity Cervids Ecosystem stability Herbivory intensity Plant communities 

Notes

Acknowledgments

This study was supported by the Norwegian Research Council under the Miljø 2015 programme (project number 204403/E40) and the Norwegian Environment Agency. Thanks to Norwegian Red Deer Centre and K.-K. Berget, P. Greve, I. G. Harstad, M. Knagenhjelm, T. R. Paulsen, T. Seldal, F. Solheim, T. Stokke, S. Vatne, V. Veiberg, T. Wiberg, K. F. Øi and H. Øyrehagen for their valuable help in the field. Sam Steyaert commented on drafts of the manuscript, and Peter Frost did copy editing. Thanks also to Mark Gillespie language help. We would like to thank the two anonymous reviewers for comments that helped improving the manuscript.

Supplementary material

11284_2016_1391_MOESM1_ESM.pdf (305 kb)
Supplementary material 1 (PDF 304 kb)

References

  1. Adler PB, Raff DA, Lauenroth WK (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128:465–479CrossRefGoogle Scholar
  2. Adrados C, Baltzinger C, Janeau G, Pepin D (2008) Red deer Cervus elaphus resting place characteristics obtained from differential GPS data in a forest habitat. Eur J Wildl Res 54:487–494. doi: 10.1007/s10344-008-0174-y CrossRefGoogle Scholar
  3. Augustine DJ, McNaughton SJ (1998) Ungulate effects on the functional species composition of plant communities: herbivore selectivity and plant tolerance. J Wildl Manage 62:1165–1183. doi: 10.2307/3801981 CrossRefGoogle 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 17:286–298. doi: 10.2981/10-038 CrossRefGoogle Scholar
  5. Bakker C, Blair JM, Knapp AK (2003) Does resource availability, resource heterogeneity or species turnover mediate changes in plant species richness in grazed grasslands? Oecologia 137:385–391. doi: 10.1007/s00442-003-1360-y CrossRefPubMedGoogle Scholar
  6. Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. https://CRAN.R-project.org/package=lme4, pp
  7. Beschta RL, Ripple WJ (2009) Large predators and trophic cascades in terrestrial ecosystems of the western United States. Biol Cons 142:2401–2414. doi: 10.1016/j.biocon.2009.06.015 CrossRefGoogle Scholar
  8. Côté SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147. doi: 10.1146/annurev.ecolsys.35.021103.105725 CrossRefGoogle Scholar
  9. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  10. DeGabriel JL, Albon SD, Fielding DA, Riach DJ, Westaway S, Irvine RJ (2011) The presence of sheep leads to increases in plant diversity and reductions in the impact of deer on heather. J Appl Ecol 48:1269–1277. doi: 10.1111/j.1365-2664.2011.02032.x CrossRefGoogle Scholar
  11. Elmqvist T, Folke C, Nystrom M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Envir 1:488–494. doi: 10.2307/3868116 CrossRefGoogle Scholar
  12. Fornara DA, du Toit JT (2007) Browsing lawns? Responses of Acacia nigrescens to ungulate browsing in an African savanna. Ecology 88:200–209. doi:10.1890/0012-9658(2007)88[200:blroan]2.0.co;2Google Scholar
  13. Frelich LE, Lorimer CG (1985) Current and predicted long-term effects of deer browsing in hemlock forests in Michigan, USA. Biol Cons 34:99–120. doi: 10.1016/0006-3207(85)90103-x CrossRefGoogle Scholar
  14. Fuller RJ, Gill RMA (2001) Ecological impacts of increasing numbers of deer in British woodland. Forestry 74:193–199. doi: 10.1093/forestry/74.3.193 CrossRefGoogle Scholar
  15. Gaston AJ, Stockton SA, Smith JL (2006) Species-area relationships and the impact of deer-browse in the complex phytogeography of the Haida Gwaii archipelago (Queen Charlotte Islands), British Columbia. Ecoscience 13:511–522. doi:10.2980/1195-6860(2006)13[511:sratio]2.0.co;2Google Scholar
  16. Godvik IMR, Loe LE, Vik JO, Veiberg V, Langvatn R, Mysterud A (2009) Temporal scales, trade-offs, and functional responses in red deer habitat selection. Ecology 90:699–710. doi: 10.1890/08-0576.1 CrossRefPubMedGoogle Scholar
  17. Heckel CD, Bourg NA, McShea WJ, Kalisz S (2010) Nonconsumptive effects of a generalist ungulate herbivore drive decline of unpalatable forest herbs. Ecology 91:319–326. doi: 10.1890/09-0628.1 CrossRefPubMedGoogle Scholar
  18. Hegland SJ, Rydgren K (2016) Eaten but not always beaten: winners and losers along a red deer herbivory gradient in boreal forest. J Veg Sci 27:111–122. doi: 10.1111/jvs.12339 CrossRefGoogle Scholar
  19. Hegland SJ, Lilleeng MS, Moe SR (2013) Old-growth forest floor richness increases with red deer herbivory intensity. For Ecol Manag 310:267–274. doi: 10.1016/j.foreco.2013.08.031 CrossRefGoogle Scholar
  20. Hester AJ, Edenius L, Buttenschon RM, Kuiters AT (2000) Interactions between forests and herbivores: the role of controlled grazing experiments. Forestry 73:381–391. doi: 10.1093/forestry/73.4.381 CrossRefGoogle Scholar
  21. Hofmann RR (1989) Evolutionanry steps of ecophysiological adaptation and diversification of ruminants: a comparative view of their digestive-system. Oecologia 78:443–457. doi: 10.1007/bf00378733 CrossRefGoogle Scholar
  22. Hovick TJ, Elmore RD, Fuhlendorf SD, Engle DM, Hamilton RG (2015) Spatial heterogeneity increases diversity and stability in grassland bird communities. Ecol Appl 25:662–672. doi: 10.1890/14-1067.1.sm CrossRefPubMedGoogle Scholar
  23. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. doi: 10.2307/3545850 CrossRefGoogle Scholar
  24. Jost L (2006) Entropy and diversity. Oikos 113:363–375. doi: 10.1111/j.2006.0030-1299.14714.x CrossRefGoogle Scholar
  25. Kindt R, Coe R (2005) Tree diversity analysis: a manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi, KenyaGoogle Scholar
  26. Koleff P, Gaston KJ, Lennon JJ (2003) Measuring beta diversity for presence-absence data. J Anim Ecol 72:367–382. doi: 10.1046/j.1365-2656.2003.00710.x CrossRefGoogle Scholar
  27. Kuijper DPJ, Jędrzejewska B, Brzeziecki B, Churski M, Jędrzejewski W, Żybura H (2010) Fluctuating ungulate density shapes tree recruitment in natural stands of the Białowieża Primeval Forest, Poland. J Veg Sci 21:1082–1098. doi: 10.1111/j.1654-1103.2010.01217.x CrossRefGoogle Scholar
  28. Kuznetsova A, Brockhoff PB, Christensen RHB (2015) lmerTest: Tests in Linear Mixed Effects Models. R package version 2.0, p 25Google Scholar
  29. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, AmsterdamGoogle Scholar
  30. MacArthur RH, Wilson EO (1963) An equilibrium theory of insular zoogeography. Evolution 17:373–387. doi: 10.2307/2407089 CrossRefGoogle Scholar
  31. Mackey RL, Currie DJ (2001) The diversity-disturbance relationship: is it generally strong and peaked? Ecology 82:3479–3492. doi:10.1890/0012-9658(2001)082[3479:tddrii]2.0.co;2Google Scholar
  32. May R (1974) Ecosystem patterns in randomly fluctuating environments. In: Rosen R, Snell F (eds) Progress in theoretical biology. Academic Press, New York, pp 1–50CrossRefGoogle Scholar
  33. Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biol Rev 88:349–364. doi: 10.1111/brv.12004 CrossRefPubMedGoogle Scholar
  34. Mysterud A, Askilsrud H, Loe LE, Veiberg V (2010) Spatial patterns of accumulated browsing and its relevance for management of red deer Cervus elaphus. Wildl Biol 16:162–172. doi: 10.2981/09-043 CrossRefGoogle Scholar
  35. Nuttle T, Ristau TE, Royo AA (2014) Long-term biological legacies of herbivore density in a landscape-scale experiment: forest understoreys reflect past deer density treatments for at least 20 years. J Ecol 102:221–228. doi: 10.1111/1365-2745.12175 CrossRefGoogle Scholar
  36. Økland R (1990) Vegetation ecology: theory, methods and applications with reference to Fennoscandia. Sommerfeltia Suppl 1:1–233Google Scholar
  37. Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richness in nutrient-poor vs. nutrient-rich ecosystems. Ecology 79:2581–2592. doi:10.1890/0012-9658(1998)079[2581:rogiop]2.0.co;2Google Scholar
  38. R Core Team (2014) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  39. Rooney TP (2009) High white-tailed deer densities benefit graminoids and contribute to biotic homogenization of forest ground-layer vegetation. Plant Ecol 202:103–111. doi: 10.1007/s11258-008-9489-8 CrossRefGoogle Scholar
  40. Rydgren K (1993) Herb-rich spruce forests in W Nordland, N Norway: an ecological and methodological study. Nordic J Bot 13:667–690. doi: 10.1111/j.1756-1051.1993.tb00112.x CrossRefGoogle Scholar
  41. Rydgren K, Økland RH, Hestmark G (2004) Disturbance severity and community resilience in a boreal forest. Ecology 85:1906–1915. doi: 10.1890/03-0276 CrossRefGoogle Scholar
  42. Sage JRW, Porter WF, Underwood HB (2003) Windows of opportunity: white-tailed deer and the dynamics of northern hardwood forests of the northeastern US. J Nat Conserv 10:213–220CrossRefGoogle Scholar
  43. Schütz M, Risch AC, Leuzinger E, Krusi BO, Achermann G (2003) Impact of herbivory by red deer (Cervus elaphus L.) on patterns and processes in subalpine grasslands in the Swiss National Park. For Ecol Manage 181:177–188. doi: 10.1016/s0378-1127(03)00131-2 CrossRefGoogle Scholar
  44. Sitters H, Di Stefano J, Christie F, Swan M, York A (2016) Bird functional diversity decreases with time since disturbance: does patchy prescribed fire enhance ecosystem function? Ecol Appl 26:115–127. doi: 10.1890/14-1562 CrossRefPubMedGoogle Scholar
  45. Skogen A, Lunde BN (1997) Flora og vegetasjon på Svanøy i Sunnfjord, med vegetasjonskart. Botanical Institute, University of Bergen, NorwayGoogle Scholar
  46. Soininen J (2010) Species turnover along abiotic and biotic gradients: patterns in space equal patterns in time? Bioscience 60:433–439. doi: 10.1525/bio.2010.60.6.7 CrossRefGoogle Scholar
  47. Steyaert S, Bokdam J, Braakhekke W, Findo S (2009) Endozoochorical plant seed dispersal by red deer (Cervus elaphus) in the Poľana Biosphere Reserve, Slovakia. Ekológia 28:191–205CrossRefGoogle Scholar
  48. Tanentzap AJ, Burrows LE, Lee WG, Nugent G, Maxwell JM, Coomes DA (2009) Landscape-level vegetation recovery from herbivory: progress after four decades of invasive red deer control. J Appl Ecol 46:1064–1072. doi: 10.1111/j.1365-2664.2009.01683.x CrossRefGoogle Scholar
  49. Tremblay JP, Huot J, Potvin F (2006) Divergent nonlinear responses of the boreal forest field layer along an experimental gradient of deer densities. Oecologia 150:78–88. doi: 10.1007/s00442-006-0504-2 CrossRefPubMedGoogle Scholar
  50. van der Maarel E (1979) Transformation of cover-abundance values in phytosociology and its effects on community similarity. Vegetatio 39:97–114. doi: 10.1007/BF00052021 CrossRefGoogle Scholar

Copyright information

© The Ecological Society of Japan 2016

Authors and Affiliations

  • Marte Synnøve Lilleeng
    • 1
    • 2
  • Stein Joar Hegland
    • 1
  • Knut Rydgren
    • 1
  • Stein R. Moe
    • 2
  1. 1.Faculty of Engineering and ScienceSogn og Fjordane University CollegeSogndalNorway
  2. 2.Department of Ecology and Natural Resource ManagementNorwegian University of Life SciencesÅsNorway

Personalised recommendations