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.
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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):904–913
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):33–48
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):1397–1406
Braun-Blanquet J (1964) Pflanzensoziologie. Springer, New York
Cain M, Milligan B, Strand A (2000) Long-distance seed dispersal in plant populations. Am J Bot 87(9):1217–1227
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):103–110
Côté SD, Rooney TP, Tremblay JP, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Evol Syst 35:113–147
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):229–236
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):204–212
De Jong T, Klinkhamer P, Boorman L (1990) Cynoglossum officinale L. J Ecol 78:1123–1144
Dickerson J, Fay P (1982) Biology and control of houndstongue (Cynoglossum officinale). In: Proceedings of the Western Society of weed science, vol 35, pp 83–85
Diekmann M (2003) Species indicator values as an important tool in applied plant ecology—a review. Basic Appl Ecol 4(6):493–506
Dony J (1977) Change in the flora of Bedfordshire, England, from 1798 to 1976. Biol Conserv 11(4):307–320
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):477–489
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):1373–1379
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.
Eschtruth A, Battles J (2009) Acceleration of exotic plant invasion in a forested ecosystem by a generalist herbivore. Conserv Biol 23(2):388–399
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):209–218
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
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):179–194
Horsley SB, Stout SL, DeCalesta DS (2003) White-tailed deer impact on the vegetation dynamics of a northern hardwood forest. Ecol Appl 13(1):98–118
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):455–464
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):110–116
Malo JE, Suarez F (1998) The dispersal of a dry-fruited shrub by red deer in a mediterranean ecosystem. Ecography 21(2):204–211
Mattocks A, Pigott C (1990) Pyrrolizidine alkaloids from Cynoglossum germanicum. Phytochemistry 29(9):2871–2872
Montserrat P, Alejandre J (2005) Los Cynoglossum, “germanicum, pustulatum & dioscoridis”, pirenaico-cantábricos. Bulletin de la Société d’histoire naturelle de Toulouse 141:31–35
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 164:263–276
R Development Core Team (2008) R: a language and environment for statistical computing. http://www.R-project.org, ISBN 3-900051-07-0
Radcliffe B (1977) A new site for the green hondstongue, Cynoglossum germanicum, in Surrey. Lond Nat 56:20–21
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, Paris
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):1–26
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):167–176
Stabell E (1995) Physiology of Cynoglossum officinale seed dormancy and germination. Master’s thesis, University of British Columbia, Vancouver, Canada
Sutory K (1988) Variability and distribution of Cynoglossum germanicum Jacq. (Boraginaceae) in western and central europe. Casopis Moravian Museum Brne 1–2:149–167
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):1345–1351
Vellend M, Knight T, Drake J (2006) Antagonistic effects of seed dispersal and herbivory on plant migration. Ecol Lett 9(3):319–326
Wang B, Smith T (2002) Closing the seed dispersal loop. Trends Ecol Evol 17(8):379–386
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 85–110
Wiser S, Allen R, Clinton P, Platt K (1998) Community structure and forest invasion by an exotic herb over 23 years. Ecology 79(6):2071–2081
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.
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Boulanger, V., Baltzinger, C., Saïd, S. et al. Deer-mediated expansion of a rare plant species. Plant Ecol 212, 307–314 (2011). https://doi.org/10.1007/s11258-010-9823-9
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DOI: https://doi.org/10.1007/s11258-010-9823-9