Skip to main content
Log in

Can browsing by deer in winter induce defence responses in bilberry (Vaccinium myrtillus)?

  • Original Article
  • Published:
Ecological Research

Abstract

Wild ungulates are key determinants in shaping boreal plant communities, and may also affect ecosystem function through inducing the plant defence systems of key plant species. We examined whether winter browsing by deer could increase the resistance of bilberry (Vaccinium myrtillus). We used three indicators of induced bilberry defence: reduced growth (a), reduced reproduction (b) and decreased insect herbivory (c) in focal plants. In a field experiment, using a randomised block design, we exposed half of plants twice in winter to exogenously applied methyl jasmonate (MeJA) and crossed this factor with randomly selecting browsed and unbrowsed plants. We predicted that MeJA-plants would have significant lower growth, reproduction and insect herbivory than Control plants. We also expected that Browsed plants would experience similar negative effects and that there would be an interaction between MeJa and Browsed indicating a possible additive effect. Growth, flowering and insect herbivory were significantly lower in MeJA than in Control, as expected. We did not find the same reduction for Browsed and no significant interaction between factors. The combined treatment, unexpectedly, flowered more and showed higher levels of insect herbivory than MeJA. Our study showed that defence responses of bilberry may be induced by exogenously-applied MeJA in winter. Our study could not confirm whether winter browsing by deer can induce the same defence responses.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Aarssen LW, Irwin DL (1991) What selection: herbivory or competition? Oikos 60:261–262. doi:10.2307/3544874

    Article  Google Scholar 

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Func Ecol 25:420–432. doi:10.1111/j.1365-2435.2010.01796.x

    Article  Google Scholar 

  • Baldwin IT (1996) Methyl jasmonate-induced nicotine production in Nicotiana attenuata: inducing defenses in the field without wounding. Entomol Exp Appl 80:213–220

    Article  CAS  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi:10.18637/jss.v067.i01

    Article  Google Scholar 

  • Bryant JP (2003) Winter browsing on Alaska feltleaf willow twigs improves leaf nutritional value for snowshoe hares in summer. Oikos 102:25–32

    Article  Google Scholar 

  • Cipollini DF, Sipe ML (2001) Jasmonic acid treatment and mammalian herbivory differentially affect chemical defenses and growth of wild mustard (Brassica kaber). Chemoecology 11:137–143. doi:10.1007/s00049-001-8319-4

    Article  CAS  Google Scholar 

  • Côte SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Ann Rev Ecol Evol Syst 35:113–147

    Article  Google Scholar 

  • Crawley M (2013) The R book, 2nd edn. Wiley, Chichester

    Google Scholar 

  • Dahlgren J, Oksanen L, Sjödin M, Olofsson J (2007) Interactions between gray-sided voles (Clethrionomys rufucanus) and bilberry (Vaccinium myrtillus), their main winter food plant. Oecologia 152:525–532

    Article  PubMed  Google Scholar 

  • Danell K, Huss-Danell K, Bergstrom R (1985) Interactions between browsing moose and two species of birch in Sweden. Ecology 66:1867–1878. doi:10.2307/2937382

    Article  Google Scholar 

  • den Herder M, Bergstrom R, Niemela P, Danell K, Lindgren M (2009) Effects of natural winter browsing and simulated summer browsing by moose on growth and shoot biomass of birch and its associated invertebrate fauna. Ann Zool Fenn 46:63–74

    Article  Google Scholar 

  • Eriksson O, Fröborg H (1996) “Windows of opportunity” for recruitment in long-lived clonal plants: experimental studies of seedling establishment in Vaccinium shrubs. Can J Bot 74:1369–1374

    Article  Google Scholar 

  • Flower-Ellis JGK (1971) Age structure and dynamics in stands of bilberry (Vaccinium myrtillus L.). PhD, Royal College of Forestry

  • Fornara DA, Du Toit JT (2008) Browsing-induced effects on leaf litter quality and decomposition in a southern African savanna. Ecosystems 11:238–249. doi:10.1007/s10021-007-9119-7

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hegland SJ, Rydgren K, Seldal T (2005) The response of Vaccinium myrtillus to variations in grazing intensity in a Scandinavian pine forest on the island of Svanøy. Can J Bot 83:1638–1644

    Article  Google Scholar 

  • Hegland SJ, Jongejans E, Rydgren K (2010) Investigating the interaction between ungulate grazing and resource effects on Vaccinium myrtillus populations with integral projection models. Oecologia 163:695–706. doi:10.1007/s00442-010-1616-2

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Hidding B, Tremblay J-P, Côté SD (2013) A large herbivore triggers alternative successional trajectories in the boreal forest. Ecology 94:2852–2860. doi:10.1890/12-2015.1

    Article  PubMed  Google Scholar 

  • Hjältén J, Danell K, Ericson L (2004) Hare and vole browsing preferences during winter. Acta Theriol 49:53–62

    Article  Google Scholar 

  • Hjeljord O, Hövik N, Pedersen HB (1990) Choice of feeding sites by moose during summer, the influence of forest structure and plant phenology. Ecography 13:281–292. doi:10.1111/j.1600-0587.1990.tb00620.x

    Article  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Ann Rev Plant Biol 59:41–66. doi:10.1146/annurev.arplant.59.032607.092825

    Article  CAS  Google Scholar 

  • Jacquemart AL (1993) Floral visitors of Vaccinium species in the high Ardennes, Belgium. Flora 188:263–273

    Google Scholar 

  • Jacquemart AL (1997) Pollen limitation in three sympatric species of Vaccinium (Ericaceae) in the upper Ardennes, Belgium. Plant Syst Evol 207:159–172

    Article  Google Scholar 

  • Jacquemart AL, Thompson JD (1996) Floral and pollination biology of three sympatric Vaccinium (Ericaceae) species in the upper Ardennes, Belgium. Can J Bot 74:210–221

    Article  Google Scholar 

  • Karban R, Yang LH, Edwards KF (2014) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52. doi:10.1111/ele.12205

    Article  PubMed  Google Scholar 

  • Kuijper DPJ, Cromsigt J, Jedrzejewska B, Miscicki S, Churski M, Jedrzejewski W, Kweczlich I (2010) Bottom-up versus top-down control of tree regeneration in the Bialowieza Primeval Forest, Poland. J Ecol 98:888–899. doi:10.1111/j.1365-2745.2010.01656.x

    Article  Google Scholar 

  • Kuusipalo J (1988) Factors affecting the fruiting of bilberries: an anlysis of categorical data set. Vegetatio 76:71–77

    Google Scholar 

  • Lindgren A, Klint J, Moen J (2007) Defense mechanisms against grazing: a study of trypsin inhibitor responses to simulated grazing in the sedge Carex bigelowii. Oikos 116:1540–1546. doi:10.1111/j.2007.0030-1299.15481.x

    Article  Google Scholar 

  • 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 21:705–716. doi:10.1111/j.1654-1103.2010.01180.x

    Google Scholar 

  • Meisingset EL, Loe LE, Brekkum Ø, Mysterud A (2014) Targeting mitigation efforts: The role of speed limit and road edge clearance for deer–vehicle collisions. J Wildl Manag 78:679–688. doi:10.1002/jwmg.712

    Article  Google Scholar 

  • Melis C, Buset A, Aarrestad PA, Hanssen O, Meisingset EL, Andersen R, Moksnes A, Roskaft E (2006) Impact of red deer Cervus elaphus grazing on bilberry Vaccinium myrtillus and composition of ground beetle (Coleoptera, Carabidae) assemblage. Biodivers Conserv 15:2049–2059

    Article  Google Scholar 

  • Milner JM, Bonenfant C, Mysterud A, Gaillard JM, Csanyi S, Stenseth NC (2006) Temporal and spatial development of red deer harvesting in Europe: biological and cultural factors. J Appl Ecol 43:721–734

    Article  Google Scholar 

  • Moen A (1999) National atlas of Norway: Vegetation. National Atlas of Norway. Norwegian Mapping Authority, Hønefoss

    Google Scholar 

  • Nykänen H, Koricheva J (2004) Damage-induced changes in woody plants and their effects on insect herbivore performance: a meta-analysis. Oikos 104:247–268. doi:10.1111/j.0030-1299.2004.12768.x

    Article  Google Scholar 

  • Pato J, Obeso JR (2013a) Effects of clipping and N fertilization on insect herbivory and infestation by pathogenic fungi on bilberry. Basic Appl Ecol 14:347–356. doi:10.1016/j.baae.2013.02.005

    Article  Google Scholar 

  • Pato J, Obeso JR (2013b) Simulated ungulate herbivory affects differently two herbivorous arthropod guilds in bilberry. Arthropod Plant Interact 7:555–565. doi:10.1007/s11829-013-9269-9

    Article  Google Scholar 

  • Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Ann Rev Cell Develop Biol 28:489–521. doi:10.1146/annurev-cellbio-092910-154055

    Article  CAS  Google Scholar 

  • Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos :244–251

  • Rodriguez-Saona C, Polashock J, Malo E (2013) Jasmonate-mediated induced volatiles in the American cranberry, Vaccinium macrocarpon: from gene expression to organismal interactions. Front Plant Sci 4:1–17. doi:10.3389/fpls.2013.00115

    Article  Google Scholar 

  • Rydgren K, Hestmark G, Økland RH (1998) Revegetation following experimental disturbance in a boreal old-growth Picea abies forest. J Veg Sci 9:763–776

    Article  Google Scholar 

  • Saetnan ER, Batzli GO (2009) Effects of simulated herbivory on defensive compounds in forage plants of Norwegian alpine rangelands. J Chem Ecol 35:469–475. doi:10.1007/s10886-009-9616-6

    Article  CAS  PubMed  Google Scholar 

  • Sampedro L, Moreira X, Zas R (2011) Costs of constitutive and herbivore-induced chemical defences in pine trees emerge only under low nutrient availability. J Ecol 99:818–827. doi:10.1111/j.1365-2745.2011.01814.x

    Article  Google Scholar 

  • Schimmel J, Granström A (1996) Fire severity and vegetation response in the boreal Swedish forest. Ecology 77:1436–1450

    Article  Google Scholar 

  • Selås V (1997) Cyclic population fluctuations of herbivores as an effect of cyclic seed cropping of plants: the mast depression hypothesis. Oikos 80:257–268

    Article  Google Scholar 

  • Selås V (2000) Population dynamics of capercaillie Tetrao urogallus in relation to bilberry Vaccinium myrtillus production in southern Norway. Wildl Biol 6:1–11

    Google Scholar 

  • Selås V (2001) Autumn population size of capercaillie Tetrao urogallus in relation to bilberry Vaccinium myrtillus production and weather: an analysis of Norwegian game reports. Wildl Biol 7:17–25

    Google Scholar 

  • Selås V (2006) Explaining bank vole cycles in southern Norway 1980–2004 from bilberry reports 1932–1977 and climate. Oecologia 147:625–631

    Article  PubMed  Google Scholar 

  • Selås V, Kobro S, Sonerud GA (2013) Population fluctuations of moths and small rodents in relation to plant reproduction indices in southern Norway. Ecosphere 4:11. doi:10.1890/es13-00228.1

    Article  Google Scholar 

  • Seldal T, Andersen KJ, Högstedt G (1994a) Grazing-induced proteinase-inhibitors: a possible cause for lemming population cycles. Oikos 70:3–11

    Article  Google Scholar 

  • Seldal T, Dybwad E, Andersen KJ, Högstedt G (1994b) Wound-induced proteinase-inhibitors in grey alder (Alnus incana)—a defense mechanism against attacking insects. Oikos 71:239–245

    Article  CAS  Google Scholar 

  • Solberg EJ et al (2012) Hjortevilt 1991–2011: Oppsummeringsrapport fra Overvåkingsprogrammet for hjortevilt. NINA, Trondheim

    Google Scholar 

  • Speed JDM, Meisingset EL, Austrheim G, Hester A, Mysterud A, Tremblay J-P, Solberg EJ (2013) Low intensities of red deer browsing constrain rowan growth in mature boreal forest of western Norway. Ecoscience 20:311–318

    Article  Google Scholar 

  • Statistics-Norway (2014) Increase in deer hunters’ yield. http://www.ssb.no/hjortejakt/. Statistics Norway. http://www.ssb.no/english/subjects/10/04/10/hjortejakt_en/. Accessed 4 April 2014

  • Strengbom J, Olofsson J, Witzell J, Dahlgren J (2003) Effects of repeated damage and fertilization on palatability of Vaccinium myrtillus to grey sided voles, Clethrionomys rufocanus. Oikos 103:133–141

    Article  Google Scholar 

  • Tolvanen A, Laine K, Pakonen T, Havas P (1994) Responses to harvesting intensity in a clonal dwarf shrub, the bilberry (Vaccinium myrtillus L.). Vegetatio 110:163–169

    Article  Google Scholar 

  • van Kleunen M, Ramponi G, Schmid B (2004) Effects of herbivory simulated by clipping and jasmonic acid on Solidago canadensis. Basic Appl Ecol 5:173–181. doi:10.1078/1439-1791-00225

    Article  Google Scholar 

  • Wegge P, Olstad T, Gregersen H, Hjeljord O, Sivkov AV (2005) Capercaillie broods in pristine boreal forest in Northwestern Russia: the importance of insects and cover in habitat selection. Can J Zool 83:1547–1555

    Article  Google Scholar 

  • Welch CA, Keay J, Kendall KC, Robbins CT (1997) Constraints on frugivory by bears. Ecology 78:1105–1119

    Article  Google Scholar 

  • White TCR (1978) The importance of a relative shortage of food in animal ecology. Oecologia 33:71–86

    Article  Google Scholar 

Download references

Acknowledgments

We would like to thank the landowner Kaupanger Hovedgård for allowing us to use their forest roads and property for research, Alison Coulthard for linguistic review, and the Research Council of Norway (Miljø 2015 programme, project number 204403/E40) and the Norwegian Environment Agency for funding.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stein Joar Hegland.

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hegland, S.J., Seldal, T., Lilleeng, M.S. et al. Can browsing by deer in winter induce defence responses in bilberry (Vaccinium myrtillus)?. Ecol Res 31, 441–448 (2016). https://doi.org/10.1007/s11284-016-1351-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11284-016-1351-1

Keywords

Navigation