Oecologia

, Volume 166, Issue 2, pp 293–303 | Cite as

Impact of herbivory on flowering behaviour and life history trade-offs in a polycarpic herb: a 10-year experiment

  • Rein Brys
  • Richard P. Shefferson
  • Hans Jacquemyn
Population ecology - Original Paper

Abstract

Herbivores can have strong deleterious effects on plant growth, reproduction, and even survival. Because these effects might be strongly interrelated, the direct consumptive effects of herbivores and a variety of indirect effects are difficult to untangle. Reductions in growth, for example, may strongly impact the flowering behaviour of plant species in the current season, but at the same time incur costs to survival, growth and reproduction in the next growing season(s). To get better insights in the effects of herbivory on the flowering behaviour of the long-lived polycarpic grassland herb Primula veris L., flowering patterns were monitored over ten consecutive years under two treatments (grazing and control mowing regimes). We tested the hypothesis that the size at flowering was affected by the presence of herbivores, and whether this translated into costs to future reproduction and survival. Overall, grazed plants were significantly smaller than control plants, and the size at which plants flowered was also significantly smaller when herbivores were present. The transition probability of flowering and of surviving into the next year was significantly smaller for all plants in the current year if they had been grazed than if they had been mown, indicating that herbivory incurred costs to both flowering and survival. Grazed plants also needed longer to start flowering, had fewer flowers and flowered less frequently, causing a significantly lower proportion of flowering adults in the population. These results suggest that the observed regression in plant size due to herbivory does not allow plants to capture enough resources to guarantee regular flowering in the longer run.

Keywords

Age of flowering Cost of reproduction Flowering frequency Iteroparity Primula veris Size-dependent flowering 

References

  1. Ackerman JD, Montalvo AM (1990) Short- and long-term limitations to fruit production in a tropical orchid. Ecology 71:263–272CrossRefGoogle Scholar
  2. Berrigan D, Koella JC (1994) The evolution of reaction norms: simple models for age and size at maturity. J Evol Biol 7:549–566CrossRefGoogle Scholar
  3. Bonser SP, Aarssen LW (2009) Interpreting reproductive allometry: individual strategies of allocation explain size-dependent reproduction in plant populations. Perspect Plant Ecol Evol Syst 11:31–40CrossRefGoogle Scholar
  4. Brody AK, Price MV, Waser NM (2007) Life-history consequences of vegetative damage in scarlet gilia, a monocarpic plant. Oikos 116:975–985CrossRefGoogle Scholar
  5. Brys R, Jacquemyn H (2009) Biological flora of the British Isles: Primula veris L. J Ecol 97:581–600CrossRefGoogle Scholar
  6. Brys R, Jacquemyn H, Endels P, De Blust G, Hermy M (2004) The effects of grassland management on plant performance and demography in the perennial herb Primula veris. J Appl Ecol 41:1080–1091CrossRefGoogle Scholar
  7. Brys R, Jacquemyn H, Endels P, De Blust G, Hermy M (2005) Effect of habitat deterioration on population dynamics and extinction risks in a previously common perennial. Conserv Biol 19:1633–1643CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (1998) Model selection and inference. Springer, New YorkGoogle Scholar
  9. Callahan HS, Pigliucci M (2002) Shade-induced plasticity and its ecological significance in wild populations of Arabidopsis thaliana. Ecology 7:1965–1980CrossRefGoogle Scholar
  10. Crawley MJ (1983) Herbivory. The dynamics of animal–plant interactions. Blackwell, OxfordGoogle Scholar
  11. de Jong TJ, Goosen-de Roo L, Klinkhamer PGL (1998) Is the threshold size for flowering in Cynoglossum officinale fixed or dependent on environment? New Phytol 138:489–496CrossRefGoogle Scholar
  12. Del-Val EK, Crawley MJ (2005) Are grazing increaser species better tolerators than decreasers? An experimental assessment of defoliation tolerance in eight British grassland species. J Ecol 93:1005–1016CrossRefGoogle Scholar
  13. Doak DF (1992) Lifetime impacts of herbivory for a perennial plant. Ecology 76:2086–2099CrossRefGoogle Scholar
  14. Ehrlén J, Van Groenendael J (2001) Storage and the delayed costs of reproduction in the understory perennial Lathyrus vernus. J Ecol 89:237–246CrossRefGoogle Scholar
  15. Ehrlén J, Syrjänen K, Leimu R, García MB, Lehtilä K (2005) Land use and population growth of Primula veris: an experimental demographic approach. J Appl Ecol 42:317–326CrossRefGoogle Scholar
  16. García MB, Ehrlén J (2002) Reproductive effort and herbivory timing in a perennial herb: fitness components at the individual and population levels. Am J Bot 89:1295–1302CrossRefGoogle Scholar
  17. Grubb PJ (1977) The maintenance of species-richness in plant communities: the importance of the regeneration niche. Biol Rev 52:107–145CrossRefGoogle Scholar
  18. Harper JL (1977) Population biology of plants. Academic, LondonGoogle Scholar
  19. Hines JE, Sauer JR (1989) Program CONTRAST: a general program for the analysis of several survival or recovery rate estimates. Fish Wildl Tech Rep 24:1–7Google Scholar
  20. Horvitz CC, Schemske DW (1988) Demographic cost of reproduction in a neotropical herb: an experimental field study. Ecology 69:1741–1745CrossRefGoogle Scholar
  21. Huntly N (1991) Herbivores and the dynamics of communities and ecosystems. Ann Rev Ecol Syst 22:477–503CrossRefGoogle Scholar
  22. Jacquemyn H, Brys R, Hermy M (2003) Short-term effects of different management regimes on the response of calcareous grassland vegetation to increased nitrogen. Biol Conserv 111:137–147CrossRefGoogle Scholar
  23. Jacquemyn H, Brys R, Jongejans E (2010) Size-dependent flowering and costs of reproduction affect population dynamics in a tuberous perennial woodland orchid. J Ecol 98:1204–1215CrossRefGoogle Scholar
  24. Kagaya M, Tani T, Kachi N (2009) Variation in flowering size and age of a facultative biennial, Aster kantoensis (Compositae), in response to nutrient availability. Am J Bot 96:1808–1813CrossRefGoogle Scholar
  25. Knight TM (2003) Effects of herbivory and its timing across populations of Trillium grandiflorum (Liliaceae). Am J Bot 90:1207–1214CrossRefGoogle Scholar
  26. Lehtilä K, Syrjänen K (1995) Positive effects of pollination on subsequent size, reproduction, and survival of Primula veris. Ecology 76:1084–1098CrossRefGoogle Scholar
  27. Lehtilä K, Syrjänen K, Leimu R, Begonã-Garcia M, Ehrlén J (2006) Habitat change and demography of Primula veris: identification of management targets. Conserv Biol 20:833–843PubMedCrossRefGoogle Scholar
  28. Leimu R, Syrjänen K, Ehrlén J, Lehtilä K (2002) Pre-dispersal seed predation in Primula veris: among-population variation in damage intensity and selection on flower number. Oecologia 133:510–516CrossRefGoogle Scholar
  29. Leon-Cortes JL, Lennon JJ, Thomas CD (2003) Ecological dynamics of extinct species in empty habitat networks. 1. The role of habitat pattern and quantity, stochasticity and dispersal. Oikos 102:449–464CrossRefGoogle Scholar
  30. Littell RC, Stroup WW, Freud RJ (2002) SAS for linear models. SAS Institute, CaryGoogle Scholar
  31. Méndez M, Karlsson PS (2004) Between population variation in size-dependent reproduction and reproductive allocation in Pinguicula vulgaris (Lentibulariaceae) and its environmental correlates. Oikos 104:59–70CrossRefGoogle Scholar
  32. Méndez M, Karlsson PS (2005) Nutrient stoichiometry in Pinguicula vulgaris: nutrient availability, plant size, and reproductive status. Ecology 86:982–991CrossRefGoogle Scholar
  33. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348CrossRefGoogle Scholar
  34. Primack R, Stacy E (1998) Cost of reproduction in the pink lady’s slipper orchid (Cypripedium acaule, Orchidaceae): an eleven-year experimental study of three populations. Am J Bot 85:1672–1679CrossRefGoogle Scholar
  35. Rees M, Sheppard A, Briese D, Mangel M (1999) Evolution of size-dependent flowering in Onopordum illyricum: a quantitative assessment of the role of stochastic selection pressures. Am Nat 154:628–651Google Scholar
  36. SAS Institute (2005) SAS onlinedoc, v.8e. SAS Institute, CaryGoogle Scholar
  37. Shefferson RP, Simms EL (2007) Costs and benefits of fruiting to future reproduction in two dormancy-prone orchids. J Ecol 95:865–875CrossRefGoogle Scholar
  38. Shefferson RP, Proper J, Beissinger SR, Simms EL (2003) Life history trade-offs in a rare orchid: the costs of flowering, dormancy, and sprouting. Ecology 84:1199–1206CrossRefGoogle Scholar
  39. Stearns SC (1992) The evolution of life histories. Oxford University Press, LondonGoogle Scholar
  40. Stearns SC, Koella JC (1986) The evolution of phenotypic plasticity in life-history traits: predictions of reaction norms for age and size at maturity. Evolution 40:893–913CrossRefGoogle Scholar
  41. Stinson KA (2004) Natural selection favors rapid reproductive phenology in Potentilla pulcherrima (Rosaceae) at opposite ends of a subalpine snowmelt gradient. Am J Bot 91:531–539CrossRefGoogle Scholar
  42. Stowe KA, Marquis RJ, Hochwender CG, Simms EL (2000) The evolutionary ecology of tolerance to consumer damage. Ann Rev Ecol Syst 31:565–595CrossRefGoogle Scholar
  43. Syrjänen K, Lehtilä K (1993) The cost of reproduction in Primula veris: differences between two adjacent populations. Oikos 67:465–472CrossRefGoogle Scholar
  44. van Noordwijk AJ, de Jong G (1986) Acquisition and allocation of resources: their influence on variation in life history tactics. Am Nat 128:137–142CrossRefGoogle Scholar
  45. Weiner J, Campbell LG, Pino J, Echarte L (2009) The allometry of reproduction within plant populations. J Ecol 97:1220–1233CrossRefGoogle Scholar
  46. Wesselingh RA, de Jong TJ (1995) Bi-directional selection on threshold size for flowering in Cynoglossum officinale (hound’s-tongue). Heredity 74:415–424Google Scholar
  47. Wesselingh RA, Klinkhamer PGL (1996) Threshold size for vernalization in Senecio jacobaea: genetic variation and response to artificial selection. Funct Ecol 10:281–288CrossRefGoogle Scholar
  48. Wesselingh RA, Klinkhamer PGL, de Jong TJ, Boorman LA (1997) Threshold size for flowering in different habitats: effects of size-dependent growth and survival. Ecology 78:2118–2132Google Scholar
  49. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46:120–138CrossRefGoogle Scholar
  50. White GC, Burnham KP, Anderson DR (2002) Advanced features of program MARK. In: Fields R (ed) Integrating people and wildlife for a sustainable future. Proceedings of the Second International Wildlife Management Congress. The Wildlife Society, Bethesda, pp 368–377Google Scholar
  51. Worley AC, Harder LD (1998) Size-dependent resource allocation and costs of reproduction in Pinguicula vulgaris (Lentibulariaceae). J Ecol 84:195–206Google Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Rein Brys
    • 1
    • 2
  • Richard P. Shefferson
    • 3
  • Hans Jacquemyn
    • 4
  1. 1.Research Institute for Nature and ForestBrusselsBelgium
  2. 2.Terrestrial Ecology Unit, Department of BiologyGhent UniversityGhentBelgium
  3. 3.University of Georgia, Odum School of EcologyAthensUSA
  4. 4.Division of Plant Ecology and Systematics, Biology DepartmentUniversity of LeuvenLeuvenBelgium

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