Plant Ecology

, Volume 196, Issue 1, pp 1–13 | Cite as

Effects of nutrient and CO2 availability on tolerance to herbivory in Brassica rapa

  • Carolyn B. Marshall
  • Germán Avila-Sakar
  • Edward G. Reekie
Article

Abstract

The ability of plants to recover from herbivore damage and maintain their fitness depends on physiological mechanisms that are affected by the availability of resources such as carbon and soil nutrients. In this study, we explored the effects of increased carbon and nutrient availability on the response of rapid cycling Brassica rapa to damage by the generalist herbivore, Trichoplusia ni (Noctuidae), in a greenhouse experiment. Using fruit mass as an estimate of plant fitness, we tested three physiological models, which predict either an increase or a decrease of tolerance to herbivory with increasing resource availability. We used leaf demography to examine some plausible mechanisms through which resource availability may affect tolerance. Our results contradict all models, and, rather, they support a more complicated view of the plasticity of resource uptake and allocation than the ones considered by the models tested. Fruit mass was negatively affected by herbivore damage only under elevated CO2, and only for certain harvest dates. Increased CO2 had no effect on the number of leaf births, but it decreased leaf longevity and the total number of leaves on a plant. Nutrient addition increased the number of leaf births, leaf longevity and the total number of leaves on a plant. We conclude that a shortening of the life span of the plants, brought about by elevated CO2, was responsible for a higher susceptibility of plants to herbivore damage under high CO2 concentration.

Keywords

Compensation Elevated CO2 Insect damage Leaf demography Growth rate model Continuum of responses model Resource limitation model 

References

  1. Addicott FT (1968) Environmental factors in the physiology of abscission. Plant Physiol 43:1471–1479PubMedGoogle Scholar
  2. Adkisson PL, Vanderzant ES, Bull DL, Allison WE (1960) A wheat germ medium for rearing the pink bollworm. J Econ Entomol 53:759–762Google Scholar
  3. Avila-Sakar G, Leist LL, Stephenson AG (2003) Effects of the spatial pattern of leaf damage on growth and reproduction: nodes and branches. J Ecol 91:867–879CrossRefGoogle Scholar
  4. Baldwin IT (1990) Herbivory simulations in ecological research. Trends Ecol Evol 5:91–93CrossRefGoogle Scholar
  5. Baldwin IT, Halitschke R, Kessler A, Schittko U (2001) Merging molecular and ecological approaches in plant–insect interactions. Curr Opin Plant Biol 4:351–358PubMedCrossRefGoogle Scholar
  6. Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta Berlin 208:137–145Google Scholar
  7. Belsky AJ (1986) Does herbivory benefit plants? A review of the evidence. Am Nat 127:870–892CrossRefGoogle Scholar
  8. Bidart-Bouzat MG (2004) Herbivory modifies the lifetime fitness response of Arabidopsis thaliana to elevated CO2. Ecology 85:297–303CrossRefGoogle Scholar
  9. Bidart-Bouzat MG, Portnoy S, de Lucia EH, Paige KN (2004) Elevated CO2 and herbivory influence trait integration in Arabidopsis thaliana. Ecol Lett 7:837–847CrossRefGoogle Scholar
  10. Boege K (2005) Influence of plant ontogeny on compensation to leaf damage. Am J Bot 92:1632–1640CrossRefGoogle Scholar
  11. Dyer MI, Turner CL, Seastedt TR (1993) Herbivory and its consequences. Ecol Appl 3:10–16CrossRefGoogle Scholar
  12. Ehrman T, Cocks PS (1996) Reproductive patterns in annual legume species on an aridity gradient. Vegetatio 122:47–59CrossRefGoogle Scholar
  13. Farnsworth EJ, Bazzaz FA (1995) Inter- and intra-generic differences in growth, reproduction, and fitness of nine herbaceous annual species grown in elevated CO2 environments. Oecologia 104:454–466CrossRefGoogle Scholar
  14. Gronemeyer PA, Dilger BJ, Bouzat JL, Paige KN (1997) The effects of herbivory on paternal fitness in scarlet gilia: better moms also make better pops. Am Nat 150:592–602CrossRefPubMedGoogle Scholar
  15. Harper JL (1977) Population biology of plants. Academic Press, LondonGoogle Scholar
  16. Hättenschwiler S, Schafellner C (1999) Opposing effects of elevated CO2 and N deposition on Lymantria monacha larvae feeding on spruce trees. Oecologia 118:210–217Google Scholar
  17. Haukioja E, Koricheva J (2000) Tolerance to herbivory in woody vs. herbaceous plants. Evol Ecol 14:551–562CrossRefGoogle Scholar
  18. Hawkes CV, Sullivan JJ (2001) The impact of herbivory on plants in different resource conditions: a meta-analysis. Ecology 82:2045–2058CrossRefGoogle Scholar
  19. Hicks S, Turkington R (2000) Compensatory growth of three herbaceous perennial species: the effects of clipping and nutrient availability. Can J Bot 78:759–767CrossRefGoogle Scholar
  20. Hilbert DW, Swift DM, Detling JK, Dyer MI (1981) Relative growth rates and the grazing optimization hypothesis. Oecologia 51:14–18CrossRefGoogle Scholar
  21. Hodgkinson KC (1974) Influence of partial defoliation on photosynthesis, photorespiration and transpiration by Lucerne leaves of different ages. Aust J Plant Physiol 1:561–578CrossRefGoogle Scholar
  22. Inouye BD, Tiffin P (2003) Measuring tolerance to herbivory with natural or imposed damage: a reply to Lehtilä. Evolution 57:681–682Google Scholar
  23. Jordan DN, Smith WK (1995) Microclimate factors influencing the frequency and duration of growth season frost for subalpine plants. Agric Forest Meteorol 77:17–30CrossRefGoogle Scholar
  24. Juenger T, Lennartsson T (2000) Tolerance in plant ecology and evolution: toward a more unified theory of plant-herbivore interaction. Evol Ecol 14:283–287CrossRefGoogle Scholar
  25. Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, ChicagoGoogle Scholar
  26. Kellogg EA, Farnsworth EJ, Russo ET, Bazzaz F (1999) Growth responses of C4 grasses of contrasting origin to elevated CO2. Annl Bot 84:279–288CrossRefGoogle Scholar
  27. Knepp RG, Hamilton JG, Mohan JE, Zangerl AR, Berenbaum MR, de Lucia EH (2005) Elevated CO2 reduces leaf damage by insect herbivores in a forest community. New Phytol 167:207–218PubMedCrossRefGoogle Scholar
  28. Lehtilä K (2003) Precision of herbivore tolerance experiments with imposed and natural damage. Evolution 57:677–682PubMedGoogle Scholar
  29. Leimu R, Koricheva J (2006) A meta-analysis of tradeoffs between plant tolerance and resistance to herbivores: combining the evidence from ecological and agricultural studies. Oikos 112:1–9CrossRefGoogle Scholar
  30. Leishman MR, Sanbrooke KJ, Woodfin RM (1999) The effects of elevated CO2 and light environment on growth and reproductive performance of four annual species. New Phytol 144:455–462CrossRefGoogle Scholar
  31. Lennartsson T, Nillsson P, Tuomi J (1998) Induction of overcompensation in the field gentian, Gentianella campestris. Ecology 79:1061–1072Google Scholar
  32. Marquis RJ (1992) The selective impact of herbivores. In: Fritz RS (ed) Plant resistance to herbivores and pathogens: ecology, evolution and genetics. University of Chicago Press, Chicago, IL, USA, pp 301–325Google Scholar
  33. Maschinski J, Whitham TG (1989) The continuum of plant responses to herbivory: the influence of plant association, nutrient availability, and timing. Am Nat 134:1–19CrossRefGoogle Scholar
  34. McIntire EJB, Hik DS (2002) Grazing history versus current grazing: leaf demography and compensatory growth of three alpine plants in response to a native herbivore. J Ecol 90:348–359CrossRefGoogle Scholar
  35. Meyer GA (1998) Mechanisms promoting recovery from defoliation in goldenrod (Solidago altissima). Can J Bot 76:450–459CrossRefGoogle Scholar
  36. Navas ML, Sonie L, Richarte J, Roy J (1997) The influence of elevated CO2 on species phenology, growth and reproduction in a Mediterranean old-field community. Global Change Biol 3:523–530CrossRefGoogle Scholar
  37. Oyama K, Geerts S, Raes D, Garcia M, Del-Castillo C, Buytaert W (1993) Geographic differentiation among populations of Arabis serrata Fr. and Sav. (Brassicaceae). J Plant Res 106:15–24CrossRefGoogle Scholar
  38. Paez A, Hellmers H, Strain BR (1980) CO2 effects on apical dominance in Pisum sativum. Physiol Plant 50:43–46CrossRefGoogle Scholar
  39. Paige KN (1999) Regrowth following ungulate herbivory in Ipomopsis aggregata: geographic evidence for overcompensation. Oecologia 118:316–323CrossRefGoogle Scholar
  40. Paige KN, Williams B, Hickox T (2001) Overcompensation through the paternal component of fitness in Ipomopsis arizonica. Oecologia 128:72–76CrossRefGoogle Scholar
  41. Pilson D (2000) The evolution of plant response to herbivory: simultaneously considering resistance and tolerance in Brassica rapa. Evol Ecol 14:457–489CrossRefGoogle Scholar
  42. Rautio P, Huhta AP, Piippo S, Tuomi J, Juenger T, Saari M, Aspi J (2005) Overcompensation and adaptive plasticity of apical dominance in Erysimum strictum (Brassicaceae) in response to simulated browsing and resource availability. Oikos 111:179–191CrossRefGoogle Scholar
  43. Reekie EG, Bazzaz FA (1991) Phenology and growth in four annual species grown in ambient and elevated CO2. Can J Bot 69:2475–2481CrossRefGoogle Scholar
  44. SAS Institute (1988) SAS user’s guide: statistics. SAS Institute Inc., Cary, NCGoogle Scholar
  45. Siemens DH, Garner SH, Mitchell-Olds T, Callaway RM (2002) Cost of defense in the context of plant competition: Brassica rapa may grow and defend. Ecology 83:505–517Google Scholar
  46. Smart CM (1994) Tansley review no. 64. Gene expression during leaf senescence. New Phytol 126:419–448CrossRefGoogle Scholar
  47. St Omer L, Hovath SM (1983) Elevated carbon dioxide concentrations and whole plant senescence. Ecology 64:1311–1314Google Scholar
  48. 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
  49. Strauss SY, Agrawal AA (1999) The ecology and evolution of plant tolerance to herbivory. Trends Ecol Evol 14:179–185PubMedCrossRefGoogle Scholar
  50. Strauss SY, Watson W, Allen MT (2003) Predictors of male and female tolerance to insect herbivory in Raphanus raphanistrum. Ecology 84:2074–2082CrossRefGoogle Scholar
  51. Thomas SC, Jasiensky M, Bazzaz FA (1999) Early vs. asymptotic growth responses of heraceous plants to elevated CO2. Ecology 80:1552–1567Google Scholar
  52. Tiffin P (2000) Mechanisms of tolerance to herbivore damage: what do we know? Evol Ecol 14:523–536CrossRefGoogle Scholar
  53. Tiffin P, Inouye BD (2000) Measuring tolerance to herbivory: accuracy and precision of estimates made using natural versus imposed damage. Evolution 54:1024–1029PubMedGoogle Scholar
  54. Trumble JT, Kolodny-Hirsch DM, Ting IP (1993) Plant compensation for arthropod herbivory. Ann Rev Entomol 38:93–119CrossRefGoogle Scholar
  55. von Ende CN (1993) Repeated-measures analysis: growth and other time-dependent measures. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Chapman & Hall, New York, pp 113–137Google Scholar
  56. Wand SJE, Midgley GF, Musil CF (1996) Growth, phenology and reproduction of an arid-environment winter ephemeral Dimorphotheca pluvialis in response to combined increases in CO2 and UV-B radiation. Environ Poll 94:247–254CrossRefGoogle Scholar
  57. Webb SE, Shelton AM (1988) Laboratory rearing of the imported cabbageworm. NY Food Life Sci Bull 122:1–6Google Scholar
  58. Whitham TG, Maschinski J, Larson KC, Paige KN (1991) Plant responses to herbivory: the continuum from negative to positive and underlying physiological mechanisms. In: Price PW (ed) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 227–256Google Scholar
  59. Wise MJ, Abrahamson WG (2005) Beyond the compensatory continuum: environmental resource levels and plant tolerance of herbivory. Oikos 109:417–428CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  • Carolyn B. Marshall
    • 1
  • Germán Avila-Sakar
    • 2
  • Edward G. Reekie
    • 1
  1. 1.Department of BiologyAcadia UniversityWolfvilleCanada
  2. 2.Biology DepartmentMount Saint Vincent UniversityHalifaxCanada

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