Advertisement

Plant Ecology

, Volume 212, Issue 2, pp 307–314 | Cite as

Deer-mediated expansion of a rare plant species

  • Vincent Boulanger
  • Christophe Baltzinger
  • Sonia Saïd
  • Philippe Ballon
  • François Ningre
  • Jean-François Picard
  • Jean-Luc Dupouey
Article

Abstract

Numerous plant colonizations have been putatively attributed to deer, based on plant species traits, fur brushing or dung analyses. But, in woodlands, direct links between the expansion of zoochorous plant species and ungulate presence have seldom been reported. Based on coupled floristic and browsing surveys, repeated in time, we analysed the causes of the spatio-temporal progression of the epizoochorous species Cynoglossum germanicum over 30 years in a network covering an 11000 ha forested area in north-eastern France. In this area, deer populations reached a peak in the 1970s, then were reduced in order to meet forest management requirements. Although initially rare and protected locally, C. germanicum has displayed an unexpected fast colonization rate during the last few decades but only in the northern part of the forest, which previously had the highest animal populations. Absent in the initial 1976 survey, C. germanicum occurred in 8% of the plots in 1981, then 46% in 2006. Logistic regression models revealed that the probability of occurrence of C. germanicum in 2006 increased not only with light indicator values, in accordance with its ecological requirements, but also with past deer browsing pressure. This result provides direct evidence of long-lasting impacts of deer populations on plant species distribution. Combining two complementary traits, animal transport and herbivory avoidance, C. germanicum benefited from epizoochorous dispersal and, once established, was protected from deer browsing by the presence of toxic proteins in its tissues. Due to the triggering role of ungulates, this species switched from the status of rare to that of colonizer within only a few decades.

Keywords

Cynoglossum germanicum Dispersal Epizoochory Modelling Spatio-temporal dynamics 

Notes

Acknowledgements

We thank P. Behr, T. Paul, C. Kieffer, D. ESilva, R. Chevalier, S. Barbier, G. Gougon, Y. Boscardin, J. Lenoir, M. LeCorre and M. Leclere for help during the fieldwork, H. Martin who made the maps, the Office National des Forêts for the lively interest they expressed in our study and V. Moore for English corrections. We also thank J.-Y. Barnagaud, A. \(\hbox{M}\dot{\hbox{a}}\hbox{rell},\) Y. Paillet and V. Pellissier for helpful comments on earlier versions of this manuscript. This study was financially supported by the French Ministry in charge of the Environment and the Office National de la Chasse et de la Faune Sauvage.

References

  1. Bartuszevige A, Endress B (2008) Do ungulates facilitate native and exotic plant spread? Seed dispersal by cattle, elk and deer in northeastern Oregon. J Arid Environ 72(6):904–913CrossRefGoogle Scholar
  2. Bossuyt B, Heyn M, Hermy M (2002) Seed bank and vegetation composition of forest stands of varying age in central Belgium: consequences for regeneration of ancient forest vegetation. Plant Ecol 162(1):33–48CrossRefGoogle Scholar
  3. Boulanger V, Baltzinger C, Saïd S, Ballon P, Picard JF, Dupouey JL (2009) Ranking temperate woody species along a gradient of browsing by deer. For Ecol Manag 258(7):1397–1406CrossRefGoogle Scholar
  4. Braun-Blanquet J (1964) Pflanzensoziologie. Springer, New YorkGoogle Scholar
  5. Cain M, Milligan B, Strand A (2000) Long-distance seed dispersal in plant populations. Am J Bot 87(9):1217–1227CrossRefPubMedGoogle Scholar
  6. Case C, Crawley M (2000) Effect of interspecific competition and herbivory on the recruitment of an invasive alien plant: Conyza sumatrensis. Biol Invas 2(2):103–110CrossRefGoogle Scholar
  7. Côté SD, Rooney TP, Tremblay JP, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147CrossRefGoogle Scholar
  8. Couvreur M, Christiaen B, Verheyen V, Hermy M (2004) Large herbivores as mobile links between isolated nature reserves through adhesive seed dispersal. Appl Veg Sci 7(2):229–236CrossRefGoogle Scholar
  9. Couvreur M, Verheyen K, Vellend M, Lamoot I, Cosyns E, Hoffmann M, Hermy M (2008) Epizoochory by large herbivores: merging data with models. Basic Appl Ecol 9(3):204–212CrossRefGoogle Scholar
  10. De Jong T, Klinkhamer P, Boorman L (1990) Cynoglossum officinale L. J Ecol 78:1123–1144CrossRefGoogle Scholar
  11. Dickerson J, Fay P (1982) Biology and control of houndstongue (Cynoglossum officinale). In: Proceedings of the Western Society of weed science, vol 35, pp 83–85Google Scholar
  12. Diekmann M (2003) Species indicator values as an important tool in applied plant ecology—a review. Basic Appl Ecol 4(6):493–506CrossRefGoogle Scholar
  13. Dony J (1977) Change in the flora of Bedfordshire, England, from 1798 to 1976. Biol Conserv 11(4):307–320CrossRefGoogle Scholar
  14. Eichberg C, Storm C, Schwabe A (2005) Epizoochorous and post-dispersal processes in a rare plant species: Jurinea cyanoides (L) Rchb(Asteraceae). Flora 200(5):477–489Google Scholar
  15. Eigenbrode S, Andreas J, Cripps M, Ding H, Biggam R, Schwarzländer M (2008) Induced chemical defenses in invasive plants: a case study with Cynoglossum officinale L. Biol Invas 10(8):1373–1379CrossRefGoogle Scholar
  16. Ellenberg H, Weber H, Dull R, Wirth V, Werner W, Paulissen D (1992) Zeigerwerte von Pflanzen in Mitteleuropa, 2nd edn, vol 18. Scripta Geobotanica 18. Verlag Erich Goltze KG, Göttingen.Google Scholar
  17. Eschtruth A, Battles J (2009) Acceleration of exotic plant invasion in a forested ecosystem by a generalist herbivore. Conserv Biol 23(2):388–399CrossRefPubMedGoogle Scholar
  18. Gill R, Beardall V (2001) The impact of deer on woodlands: the effects of browsing and seed dispersal on vegetation structure and composition. Forestry 74(3):209–218CrossRefGoogle Scholar
  19. Harrell F (2008) Design: Design Package. http://www.biostat.mc.vanderbilt.edu/s/Design, http://www.biostat.mc.vanderbilt.edu/rms, r package version 2.1-2
  20. Heinken T, Raudnitschka D (2002) Do wild ungulates contribute to the dispersal of vascular plants in central european forests by epizoochory? A case study in NE Germany. Forstwissenschaftliches Centralblatt 121(4):179–194CrossRefGoogle Scholar
  21. Horsley SB, Stout SL, DeCalesta DS (2003) White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecol Appl 13(1):98–118CrossRefGoogle Scholar
  22. Hovstad K, Borvik S, Ohlson M (2009) Epizoochorous seed dispersal in relation to seed availability—an experiment with a red fox dummy. J Veg Sci 20(3):455–464CrossRefGoogle Scholar
  23. Knight TM, Dunn JL, Smith LA, Davis J, Kalisz S (2009) Deer facilitate invasive plant success in a Pennsylvania forest understory. Nat Areas J 29(2):110–116CrossRefGoogle Scholar
  24. Malo JE, Suarez F (1998) The dispersal of a dry-fruited shrub by red deer in a mediterranean ecosystem. Ecography 21(2):204–211CrossRefGoogle Scholar
  25. Mattocks A, Pigott C (1990) Pyrrolizidine alkaloids from Cynoglossum germanicum. Phytochemistry 29(9):2871–2872CrossRefGoogle Scholar
  26. Montserrat P, Alejandre J (2005) Los Cynoglossum, “germanicum, pustulatum & dioscoridis”, pirenaico-cantábricos. Bulletin de la Société d’histoire naturelle de Toulouse 141:31–35Google Scholar
  27. Nomiya H, Suzuki W, Kanazashi T, Shibata M, Tanaka H, Nakashizuka T (2002) The response of forest floor vegetation and tree regeneration to deer exclusion and disturbance in a riparian deciduous forest, central Japan. Plant Ecol 164:263–276CrossRefGoogle Scholar
  28. R Development Core Team (2008) R: a language and environment for statistical computing. http://www.R-project.org, ISBN 3-900051-07-0
  29. Radcliffe B (1977) A new site for the green hondstongue, Cynoglossum germanicum, in Surrey. Lond Nat 56:20–21Google Scholar
  30. Rameau J, Mansion D, Dumé G, Lecointe A, Timbal J, Dupont P, Keller R (1993) Flore Forestière Française; Guide écologique illustré; II; Montagnes. Institut de développement forestier, ParisGoogle Scholar
  31. Russell FL, Zippin DB, Fowler NL (2001) Effects of white-tailed deer (Odocoileus virginianus) on plants, plant populations and communities: a review. Am Midland Nat 146(1):1–26CrossRefGoogle Scholar
  32. Schmidt M, Sommer K, Kriebitzsch W, Ellenberg H, von Oheimb G (2004) Dispersal of vascular plants by game in northern Germany; Part I: roe deer (Capreolus capreolus) and wild boar (Sus scrofa). Eur J For Res 123(2):167–176Google Scholar
  33. Stabell E (1995) Physiology of Cynoglossum officinale seed dormancy and germination. Master’s thesis, University of British Columbia, Vancouver, CanadaGoogle Scholar
  34. Sutory K (1988) Variability and distribution of Cynoglossum germanicum Jacq. (Boraginaceae) in western and central europe. Casopis Moravian Museum Brne 1–2:149–167Google Scholar
  35. Valéry L, Fritz H, Lefeuvre J, Simberloff D (2008) In search of a real definition of the biological invasion phenomenon itself. Biol Invas 10(8):1345–1351CrossRefGoogle Scholar
  36. Vellend M, Knight T, Drake J (2006) Antagonistic effects of seed dispersal and herbivory on plant migration. Ecol Lett 9(3):319–326CrossRefPubMedGoogle Scholar
  37. Wang B, Smith T (2002) Closing the seed dispersal loop. Trends Ecol Evol 17(8):379–386CrossRefGoogle Scholar
  38. Willson M, Traveset A (2000) The ecology of seed dispersal. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities, vol 2. CABI Publishing, Wallingford, pp 85–110CrossRefGoogle Scholar
  39. Wiser S, Allen R, Clinton P, Platt K (1998) Community structure and forest invasion by an exotic herb over 23 years. Ecology 79(6):2071–2081CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Vincent Boulanger
    • 1
    • 2
    • 3
    • 4
  • Christophe Baltzinger
    • 3
  • Sonia Saïd
    • 4
  • Philippe Ballon
    • 3
  • François Ningre
    • 5
  • Jean-François Picard
    • 2
  • Jean-Luc Dupouey
    • 2
  1. 1.Laboratoire d’Ecologie, EA 1293 ECODIV, UFR Sciences et TechniquesUniversité de RouenMont-Saint-AignanFrance
  2. 2.UMR 1137 Écologie et Écophysiologie ForestièresINRA – Université Nancy 1 Route d’AmanceChampenouxFrance
  3. 3.Cemagref, Gestion des TerritoiresNogent-sur-VernissonFrance
  4. 4.ONCFS, CNERA Cervidés-sanglierBirieuxFrance
  5. 5.UMR 1092 Laboratoire d’Etude des Ressources Forêt-BoisINRA – AgroParisTech ENGREF Route d’AmanceChampenouxFrance

Personalised recommendations