Ecological Research

, Volume 22, Issue 4, pp 671–677

Carbon–nitrogen stoichiometry in the tritrophic food chain willow, leaf beetle, and predatory ladybird beetle

Original Article

Abstract

Although plant quality can indirectly increase the performance of the third trophic level by bottom-up cascading effects, the mechanisms of this indirect effect are still unclear. In this study the carbon–nitrogen stoichiometry in a tri-trophic system consisting of the willow, a leaf beetle, and a predatory ladybird beetle were examined to determine the mechanisms of the bottom-up cascading effect. The bottom-up cascade is initiated by increasing leaf nitrogen, because of artificial cutting of willow trees. The relative growth rate (RGR) of the leaf beetle increased when fed on cut willow leaves, because of the high leaf nitrogen in the cut willows. Ladybird beetle RGR also increased when fed on leaf beetles fed on cut willow leaves. The increased RGR of the ladybirds cannot be explained by the quality of the prey, however, because leaf beetle nitrogen was not affected by host plant quality. Thus, the carbon–nitrogen stoichiometry could not be a mechanism of the bottom-up cascade through multiple trophic levels.

Keywords

Bottom-up cascade C:N ratio Ecological stoichiometry Terrestrial food chain Tri-trophic interaction 

References

  1. Anderson T, Hessen DO (1991) Carbon, nitrogen, and phosphorus concentration of freshwater zooplankton. Limnol Oceanogr 36:807–814CrossRefGoogle Scholar
  2. Cotrufo MF, Ineson P, Scott A (1998) Elevated CO2 reduces the nitrogen concentration of plant tissues. Glob Change Biol 4:43–54CrossRefGoogle Scholar
  3. Crone EE, Jones CG (1999) The dynamics of carbon–nutrient balance: effects of cottonwood acclimation to short-and long-term shade on beetle feeding preferences. J Chem Ecol 25:635–656CrossRefGoogle Scholar
  4. Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods. Ecology 84:2522–2531CrossRefGoogle Scholar
  5. Faeth SH (1986) Indirect interactions between temporally separated herbivores mediated by the host plant. Ecology 67:479–494CrossRefGoogle Scholar
  6. Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802CrossRefPubMedGoogle Scholar
  7. Feeny P (1970) Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51:555–581CrossRefGoogle Scholar
  8. Harvey JA, Van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531CrossRefGoogle Scholar
  9. Haukioja E, Niemelä P, Sirén S (1985) Foliage phenols and nitrogen in relation to growth, insect damage, and ability to recover after defoliation, in the mountain birch Betura pubescens ssp tortuosa. Oecologia 65:214–222CrossRefGoogle Scholar
  10. Hikosaka K, Takashima T, Kabeya D, Hirose T, Kamata N (2005) Biomass allocation and leaf chemical defense in defoliated seedlings of Quercus serrata with respect to carbon–nitrogen balance. Ann Bot 95:1025–1032PubMedCrossRefGoogle Scholar
  11. Hunter MD (2003) Effects of plant quality on the population ecology of parasitoids. Agric For Entomol 5:1–8CrossRefGoogle Scholar
  12. Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural community. Ecology 73:724–732Google Scholar
  13. Kagata H, Katayama N (2006) Does nitrogen limitation promote intraguild predation in an aphidophagous ladybird? Entomol Exp Appl 119:239–246CrossRefGoogle Scholar
  14. Kagata H, Ohgushi T (2006) Nitrogen homeostasis in a willow leaf beetle, Plagiodera versicolora, independence of host plant quality. Entomol Exp Appl 118:105–110CrossRefGoogle Scholar
  15. Kagata H, Nakamura M, Ohgushi T (2005) Bottom-up cascade in a tri-trophic system: different impacts of host–plant regeneration on performance of a willow leaf beetle and its natural enemy. Ecol Entomol 30:58–62CrossRefGoogle Scholar
  16. Kimoto S, Takizawa H (1994) Leaf beetles (Chrysomelidae) of Japan. Tokai University Press, TokyoGoogle Scholar
  17. Kimura Y (1989) Salicaceae. In: Satake Y, Hara H, Watari S, Tominari T (eds) Wild flowers of Japan. Woody plants Heibonsha, Tokyo, pp 31–51Google Scholar
  18. Kudo G (2003) Variations in leaf traits and susceptibility to insect herbivory within a Salix miyabeana population under field conditions. Plant Ecol 169:61–69CrossRefGoogle Scholar
  19. Lower SS, Orians CM (2003) Soil nutrients and water availability interact to influence willow growth and chemistry but not leaf beetle performance. Entomol Exp Appl 107:69–79CrossRefGoogle Scholar
  20. Makino W, Cotner JB (2004) Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implications for growth-and resource-dependent variations. Aquat Microb Ecol 34:33–41Google Scholar
  21. Martinsen GD, Driebe EM, Whitham TG (1998) Indirect interactions mediated by changing plant chemistry: beaver browsing benefits beetles. Ecology 79:192–200CrossRefGoogle Scholar
  22. Matsumura M, Trafelet-Smith GM, Gratton C, Finke DL, Fagan WE, Denno RF (2004) Does intraguild predation enhance predator performance? A stoichiometric perspective. Ecology 85:2601–2615CrossRefGoogle Scholar
  23. Matsura T (1976) Ecological studies of a coccinellid, Aiolocaria hexaspilota Hope. I. Interaction between field populations of A. hexaspilota and its prey, the walnut leaf beetle (Gastrolina depressa Baly). Jpn J Ecol 26:147–156 (in Japanese)Google Scholar
  24. Mattson WJ (1980) Herbivory in relation to plant nitrogen concentration. Ann Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  25. Mattson WJ, Scriber JM (1987) Nutritional ecology of insect folivores of woody plants: nitrogen, water, fiber, and mineral considerations. In: Slansky F, Rodrigues JG (eds) Nutritional ecology of insects, mites, spiders, and related invertebrates. Wiley, New York, pp 105–146Google Scholar
  26. Mayntz D, Toft S (2001) Nutrient composition of the prey’s diet affects growth and survivorship of a generalist predator. Oecologia 127:207–213CrossRefGoogle Scholar
  27. Nomura M, Itioka T (2002) Effects of synthesized tannin on the growth and survival of a generalist herbivorous insect, the common cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Appl Entomol Zool 37:285–289CrossRefGoogle Scholar
  28. Obermaier E, Zwölfer H (1999) Plant quality or quantity? Host exploitation strategies in three Chrysomelidae species associated with Asteraceae host plants. Entomol Exp Appl 92:165–177CrossRefGoogle Scholar
  29. Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Ann Rev Ecol Syst 11:41–65CrossRefGoogle Scholar
  30. Raubenheimer D, Simpson SJ (2004) Organismal stoichiometry: quantifying non-independence among food components. Ecology 85:1203–1216CrossRefGoogle Scholar
  31. Raupp MJ, Denno RF (1983) Leaf age as a predictor of herbivore distribution and abundance. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic, New York, pp 91–124Google Scholar
  32. Simpson SJ, Raubenheimer D (2001) The geometric analysis of nutrient–allelochemical interactions: a case study using locusts. Ecology 82:422–439Google Scholar
  33. Slansky F, Feeny P (1977) Stabilization of the rate of nitrogen accumulation by larvae of the cabbage butterfly on wild and cultivated food plants. Ecol Monogr 47:209–228CrossRefGoogle Scholar
  34. Sterner RW, Elser JJ (2002) Ecological stoichiometry. Princeton University Press, PrincetonGoogle Scholar
  35. Teder T, Tammaru T (2002) Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids. Ecol Entomol 27:94–104CrossRefGoogle Scholar
  36. Toft S, Wise DH (1999) Growth, development, and survival of a generalist predator fed single- and mixed-species diets of different quality. Oecologia 119:191–197CrossRefGoogle Scholar
  37. White TCR (1993) The inadequate environment. Springer, Berlin Heidelberg New YorkGoogle Scholar

Copyright information

© The Ecological Society of Japan 2006

Authors and Affiliations

  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan

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