Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Tolerance of a perennial herb, Pimpinella saxifraga, to simulated flower herbivory and grazing: immediate repair of injury or postponed reproduction?

  • 198 Accesses

  • 26 Citations

Abstract

Perennial, polycarpic herbs can respond to herbivory either by (1) regrowth in the same season in order to compensate for lost reproductive structures or by (2) postponing reproduction until the following growing season. We tested these response patterns with the perennial umbellifer Pimpinella saxifraga by simulating flower herbivory and shoot grazing both in the field and in a common garden experiment. In the field, both simulated flower herbivory and grazing effectively suppressed current reproduction, whereas no statistically significant effects of previous-year treatments on growth or reproduction were found in the following year. In the common garden, in the first year the species fully compensated for simulated flower herbivory in vegetative parameters but seed set was reduced by 26%. After 2 years of flower removal, the plants overcompensated in shoot and root biomass by 47 and 46%, respectively, and compensated fully in reproductive performance. Simulated grazing resulted in 21% lower shoot biomass in the first season, but the root biomass was not affected. In the second season the root biomass increased by 43% as compared to the control plants. However, regrowth following simulated grazing resulted in a significant delay in flowering with the consequence that the seed yield of fertile plants was reduced by 55% as compared to the control plants. These results suggest that in resource-rich garden conditions P. saxifraga may immediately repair injuries caused by flower herbivory, but repairs more extensive shoot injury less successfully. Delayed phenology decreases the benefits of immediate repair. In resource-poor conditions, the benefits of regrowth can be negligible. Accordingly, in our field population, the plants postponed their reproduction until the following year in response to simulated grazing and frequently in response to flower removal. When the plants gain very little from regrowth, the costs of reproduction would select for postponed reproduction in response to injury.

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

Fig. 1
Fig. 2
Fig. 3

References

  1. Belsky AJ (1986) Does herbivory benefits plants? A review of evidence. Am Nat 127:870–892. doi:10.1086/284531

  2. Benner BL (1988) Effects of apex removal and nutrient supplementation on branching and seed production in Thlaspi arvense (Brassicaceae). Am J Bot 75:645–651. doi:10.2307/2444198

  3. Bergelson J, Crawley MJ (1992) Herbivory and Ipomopsis aggregata the disadvantages of being eaten. Am Nat 139:870–882. doi:10.1086/285362

  4. Caswell H (1989) Matrix population models. Sinauer, Sunderland

  5. Cornu A, Carnat A-P, Martin B, Coulon J-B, Lamaison J-L, Berdaque J-L (2001) Solid-phase microextraction on volatile components from natural grassland plants. J Agric Food Chem 49:203–209. doi:10.1021/jf0008341

  6. Cox CS, McEvoy PB (1983) Effect of summer moisture stress on the capacity of tansy ragwort (Senecio jacobaea) to compensate for defoliation by cinnabar moth (Tyria jacobaeae). J Appl Ecol 20:225–234. doi:10.2307/2403388

  7. Grime JP, Hodgson JG, Hunt R (1988) Comparative plant ecology. A functional approach to common British species. Unwin Hyman, London

  8. Hämet-Ahti L (1980) Pukinjuuri—Pimpinella saxifraga L. In: Jalas J (ed) Suuri kasvikirja III. Otava, Keuruu, pp 216–217

  9. Hemborg AM (1998) Cost of reproduction in subarctic Ranunculus acris: a five-year field experiment. Oikos 83:273–282. doi:10.2307/3546838

  10. Hendrix SD, Trapp EJ (1989) Floral herbivory in Pastinaca sativa: do compensatory responses offset reductions in fitness. Evolution 43:891–895

  11. Houle G (2001) Reproductive costs are associated with both male and female functions in Alnus viridis ssp. crispa. Ecoscience 8:220–229

  12. Huhta A-P, Hellström K, Rautio P, Tuomi J (2000a) A test of the compensatory continuum: fertilization increases and below-ground competition decreases tolerance of tall wormseed mustard (Erysimum strictum). Evol Ecol 14:353–372. doi:10.1023/A:1010808925284

  13. Huhta A-P, Lennartsson T, Tuomi J, Rautio P, Laine K (2000b) Tolerance of Gentianella campestris in relation to damage intensity: an interplay between apical dominance and herbivory. Evol Ecol 14:373–392. doi:10.1023/A:1011028722860

  14. Jantunen J, Saarinen K (2003) A comparison of vegetation in grazed, formerly grazed and ungrazed valuable semi-natural grasslands in SE Finland. Memoranda Societatis Fauna Flora Fenn 78:55–61

  15. Juenger T, Bergelson J (1997) Pollen and resource limitation of compensation to herbivory in scarlet gilia, Ipomopsis aggregata. Ecology 78:1684–1695

  16. Kalela A, Väänänen H (1960) Pimpinella saxifraga L. Tavallinen pukinjuuri. In: Kalela A, Väänänen H (eds) Pohjolan luonnonkasvit 3. WSOY, Porvoo, pp 1328–1330

  17. Karban R, Strauss SH (1993) Effects of herbivores on growth and reproduction of their perennial host, Erigeron glaucus. Ecology 74:39–46. doi:10.2307/1939499

  18. Knight TM (2003) Effects of herbivory and its timing across populations of Trillium grandiflorum (Liliaceae). Am J Bot 90:1207–1214. doi:10.3732/ajb.90.8.1207

  19. Lennartsson T, Nilsson P, Tuomi J (1998) Induction of overcompensation in the field gentian, Gentianella campestris. Ecology 79:1061–1072

  20. Levine MT, Paige KN (2004) Direct and indirect effects of drought on compensation following herbivory in scarlet gilia. Ecology 85:3185–3191. doi:10.1890/03-0748

  21. Louda SM (1984) Herbivore effect on stature, fruiting, and leaf dynamics of a native crucifer. Ecology 65:1379–1386

  22. Marttila O, Haahtela T, Aarnio H, Ojalainen P (1990) Suomen päiväperhoset, (Finnish Butterflies). Kirjayhtymä, Helsinki

  23. Maschinski J, Whitham GT (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability and timing. Am Nat 134:1–19. doi:10.1086/284962

  24. McNaughton SJ (1983) Compensatory plant growth as a response to herbivory. Oikos 40:329–336. doi:10.2307/3544305

  25. McNaughton SJ, Banyikwa FF, McNaughton MM (1998) Root biomass and productivity in a grazing ecosystem: the Serengeti. Ecology 79:587–592

  26. Newman JA, Bergelson J, Grafen A (1997) Blocking factors and hypothesis testing in ecology: is your statistics text wrong? Ecology 78:1312–1320

  27. Nilsson P, Tuomi J, Åström P (1996) Bud dormancy as a bet-hedging strategy. Am Nat 147:269–281. doi:10.1086/285849

  28. Obeso JR (2002) The costs of reproduction in plants. New Phytol 155:321–348. doi:10.1046/j.1469-8137.2002.00477.x

  29. Paige KN, Whitham TG (1987) Flexible life history traits: shifts by Scarlet gilia in response to pollinator abundance. Ecology 68:1691–1695. doi:10.2307/1939861

  30. Rosenthal JP, Kotanen PM (1994) Terrestrial plant tolerance to herbivory. Trends Ecol Evol 9:145–148. doi:10.1016/0169-5347(94)90180-5

  31. Sadras VO (1996) Cotton compensatory growth after loss of reproductive organs as affected by availability of resources and duration of recovery period. Oecologia 106:432–439. doi:10.1007/BF00329698

  32. Scheiner SM (1993) MANOVA: multiple response variables and multispecies interactions. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman and Hall, New York, pp 94–112

  33. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185. doi:10.1016/S0169-5347(98)01576-6

  34. Tolvanen A, Laine K (1997) Effects of reproduction and artificial herbivory on vegetative growth and resource levels in deciduous and evergreen dwarf shrubs. Can J Bot 75:656–666

  35. Trumble JT, Kolodny-Hirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Annu Rev Entomol 38:93–119. doi:10.1146/annurev.en.38.010193.000521

  36. Vail SP (1992) Selection for overcompensatory plant responses to herbivory: a mechanism for the evolution of plant-herbivore mutualism. Am Nat 139:1–8. doi:10.1086/285309

  37. Venecz JI, Aarssen LW (1998) Effects of shoot apex removal in Lythrum salicaria (Lythraceae): assessing the costs of reproduction and apical dominance. Ann Bot Fenn 35:101–111

  38. Wells TCE, Sheail J, Ball DL, Ward LK (1976) Ecological studies on the Porton ranges: relationships between vegetation, soils and land-use history. J Ecol 64:589–626. doi:10.2307/2258775

  39. Whitham TG, Maschinski J, Larson KC, Paige KN (1991) Plant responses to herbivory: the continuum form negative to positive and underlying physiological mechanisms. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 227–256

  40. Wise MJ, Cummins JJ, De Young C (2008) Compensation for floral herbivory in Solanum carolinense: identifying mechanisms of tolerance. Evol Ecol 22:19–37. doi:10.1007/s10682-007-9156-x

Download references

Acknowledgements

The work was financially supported by the Academy of Finland (projects #40951 and #80486), the Emil Aaltonen Foundation and Kone Foundation. We thank the technical staff of Oulanka Research Station and Department of Biology at the University of Oulu for their valuable help in the field and laboratory. Aaron Bergdahl kindly checked the language. Finally, sincerest thanks to S.-M. Horttanainen for her field assistance.

Author information

Correspondence to A-P. Huhta.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Huhta, A., Rautio, P., Hellström, K. et al. Tolerance of a perennial herb, Pimpinella saxifraga, to simulated flower herbivory and grazing: immediate repair of injury or postponed reproduction?. Plant Ecol 201, 599–609 (2009). https://doi.org/10.1007/s11258-008-9535-6

Download citation

Keywords

  • Burnet saxifrage
  • Cost of herbivory
  • Cost of reproduction
  • Fitness
  • Plant life-history
  • Tolerance