, Volume 152, Issue 2, pp 265–273 | Cite as

Nurse plants, tree saplings and grazing pressure: changes in facilitation along a biotic environmental gradient

  • Christian SmitEmail author
  • Charlotte Vandenberghe
  • Jan den Ouden
  • Heinz Müller-Schärer
Plant Animal Interaction


Current conceptual models predict that an increase in stress shifts interactions between plants from competitive to facilitative; hence, facilitation is expected to gain in ecological importance with increasing stress. Little is known about how facilitative interactions between plants change with increasing biotic stress, such as that incurred by consumer pressure or herbivory (i.e. disturbance sensu Grime). In grazed ecosystems, the presence of unpalatable plants is reported to protect tree saplings against cattle grazing and enhance tree establishment. In accordance with current conceptual facilitation-stress models, we hypothesised a positive relationship between facilitation and grazing pressure. We tested this hypothesis in a field experiment in which tree saplings of four different species (deciduous Fagus sylvatica, Acer pseudoplatanus and coniferous Abies alba, Picea abies) were planted either inside or outside of the canopy of the spiny nurse shrub Rosa rubiginosa in enclosures differing in grazing pressure (low and high) and in exclosures. During one grazing season we followed the survival of the different tree saplings and the level of browsing on these; we also estimated browsing damage to the nurse shrubs. Shrub damage was highest at the higher grazing pressure. Correspondingly, browsing increased and survival decreased in saplings located inside the canopy of the shrubs at the high grazing pressure compared to the low grazing pressure. Saplings of both deciduous species showed a higher survival than the evergreens, while sapling browsing did not differ between species. The relative facilitation of sapling browsing and sapling survival – i.e. the difference between saplings inside and outside the shrub canopy – decreased at high grazing pressure as the facilitative species became less protective. Interestingly, these findings do not agree with current conceptual facilitation-stress models predicting increasing facilitation with abiotic stress. We used our results to design a conceptual model of facilitation along a biotic environmental gradient. Empirical studies are needed to test the applicability of this model. In conclusion, we suggest that current conceptual facilitation models should at least consider the possibility of decreasing facilitation at high levels of stress.


Cattle grazing Facilitation theory Herbivory Nurse effects Unpalatable plants 



We are grateful to the agronomic research station of Agroscope Changins (RAC) for allowing us to use la Petite Ronde as field site and for helping us set up the exclosures. Further, we thank C. Rosat for his help with transplanting the shrubs and trees, F. Freléchoux and R. Smit for their help and advice during this study and M. Pohl for her extensive help with gathering the data. We thank M. Holmgren for improving this manuscript with useful comments. This project was funded by the National Centre of Competence in Research (NCCR) Plant Survival of the Swiss National Science Foundation.


  1. Atstatt PR, Odowd DJ (1976) Plant defense guilds. Science 193:24–29CrossRefGoogle Scholar
  2. Bakker ES, Olff H, Vandenberghe C, De Maeyer K, Smit R, Gleichman JM, Vera FWM (2004) Ecological anachronisms in the recruitment of temperate light-demanding tree species in wooded pastures. J Appl Ecol 41:571–582CrossRefGoogle Scholar
  3. Bergman M, Iason GR, Hester AJ (2005) Feeding patterns by roe deer and rabbits on pine, willow and birch in relation to spatial arrangement. Oikos 109:513–520CrossRefGoogle Scholar
  4. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193CrossRefGoogle Scholar
  5. Bertness MD, Ewanchuk PJ (2002) Latitudinal and climate-driven variation in the strength and nature of biological interactions in New England salt marshes. Oecologia 132:392–401CrossRefGoogle Scholar
  6. Bokdam J (2003) Nature conservation and grazing management. Free ranging cattle as a driving force for cyclic vegetation succession. PUDOC, Wageningen University, WageningenGoogle Scholar
  7. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125CrossRefGoogle Scholar
  8. Callaway RM, Walker LR (1997) Competition and facilitation: a synthetic approach to interactions in plant communities. Ecology 78:1958–1965CrossRefGoogle Scholar
  9. Callaway RM, Brooker RW, Choler P, Kikvidze Z, Lortie CJ, Michalet R, Paolini L, Pugnaire FI, Newingham B, Aschehoug ET, Armas C, Kikodze D, Cook BJ (2002) Positive interactions among alpine plants increase with stress. Nature 417:844–848PubMedCrossRefGoogle Scholar
  10. Choler P, Michalet R, Callaway RM (2001) Facilitation and competition on gradients in alpine plant communities. Ecology 82:3295–3308CrossRefGoogle Scholar
  11. Crawley MJ (1983) Herbivory. Studies in ecology, vol. 10. The dynamics of animal–plant interactions. Blackwell, OxfordGoogle Scholar
  12. Flores J, Jurado E (2003) Are nurse–protégé interactions more common among plants from arid environments? J Veg Sci 14:911–916CrossRefGoogle Scholar
  13. Franks SJ (2003) Facilitation in multiple life-history stages: evidence for nucleated succession in coastal dunes. Plant Ecol 168:1–11CrossRefGoogle Scholar
  14. Gomez-Aparicio L, Zamora R, Gomez JM, Hodar JA, Castro J, Baraza E (2004) Applying plant facilitation to forest restoration: a meta-analysis of the use of shrubs as nurse plants. Ecol Appl 14:1128–1138Google Scholar
  15. Grime JP (1977) Evidence for existence of 3 primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:169–1194CrossRefGoogle Scholar
  16. Hall LM, George MR, McCreary DD, Adams TE (1992) Effects of cattle grazing on blue oak seedling damage and survival. J Range Manage 45:503–506Google Scholar
  17. Hambäck PA, Ågren J, Ericson L (2000) Associational resistance: insect damage to purple loosestrife reduced in thickets of sweet gale. Ecology 81:1784–1794CrossRefGoogle Scholar
  18. Hester AJ, Millard P, Baillie GJ, Wendler R (2004) How does timing of browsing affect above- and below-ground growth of Betula pendula, Pinus sylvestris and Sorbus aucuparia? Oikos 105:536–550CrossRefGoogle Scholar
  19. Holmgren M, Scheffer M, Huston MA (1997) The interplay of facilitation and competition in plant communities. Ecology 78:1966–1975CrossRefGoogle Scholar
  20. Kareiva PM, Bertness MD (1997) Re-examining the role of positive interactions in communities. Ecology 78:1945CrossRefGoogle Scholar
  21. Krause SC, Raffa KF (1996) Differential growth and recovery rates following defoliation in related deciduous and evergreen trees. Trees-Struct Funct 10:308–316Google Scholar
  22. Liss BM (1988) Der Einfluss von weidevieh und wild auf die natürliche und künstliche Verjüngung im Bergmischwald der ostbayerischen Alpen. Forstwiss Cbl 107: 14–25Google Scholar
  23. Maestre FT, Valladares F, Reynolds JF (2005) Is the change of plant–plant interactions with abiotic stress predictable? A meta-analysis of field results in arid environments. J Ecol 93:748–757CrossRefGoogle Scholar
  24. Milchunas DG, Noy-Meir I (2002) Grazing refuges, external avoidance of herbivory and plant diversity. Oikos 99:113–130CrossRefGoogle Scholar
  25. Rousset O, Lepart J (2000) Positive and negative interactions at different life stages of a colonizing species (Quercus humilis). J Ecol 88:401–412CrossRefGoogle Scholar
  26. Shumway SW (2000) Facilitative effects of a sand dune shrub on species growing beneath the shrub canopy. Oecologia 124:138–148CrossRefGoogle Scholar
  27. Smit C, Béguin D, Buttler A, Mueller-Schaerer H (2005) Safe sites for tree regeneration in wooded pastures: a case of associational resistance? J Veg Sci 16:209–214CrossRefGoogle Scholar
  28. Smit C, den Ouden J, Mueller-Schaerer H (2006) Unpalatable plants facilitate tree sapling survival in wooded pastures. J Appl Ecol 43:305–312CrossRefGoogle Scholar
  29. Tewksbury JJ, Lloyd JD (2001) Positive interactions under nurse-plants: spatial scale, stress gradients and benefactor size. Oecologia 127:425–434CrossRefGoogle Scholar
  30. Tirado R, Pugnaire FI (2003) Shrub spatial aggregation and consequences for reproductive success. Oecologia 136:296–301PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Christian Smit
    • 1
    • 4
    Email author
  • Charlotte Vandenberghe
    • 2
  • Jan den Ouden
    • 3
  • Heinz Müller-Schärer
    • 1
  1. 1.Department of Biology, Unit of Ecology and EvolutionUniversity of FribourgFribourgSwitzerland
  2. 2.Swiss Federal Research Institute WSLLausanneSwitzerland
  3. 3.Centre for Ecosystem Studies, Forest Ecology and Forest Management GroupWageningen UniversityWageningenThe Netherlands
  4. 4.Community and Conservation Ecology group, Centre for Ecological and Evolutionary studiesUniversity of Groningen HarenThe Netherlands

Personalised recommendations