, Volume 137, Issue 1, pp 32–41 | Cite as

Effects of light and nutrient availability on the growth, allocation, carbon/nitrogen balance, phenolic chemistry, and resistance to herbivory of two freshwater macrophytes

  • Greg CroninEmail author
  • David M. Lodge


Phenotypic responses of Potamogeton amplifolius and Nuphar advena to different light (7% and 35% of surface irradiance) and nutrient environments were assessed with field manipulation experiments. Higher light and nutrient availability enhanced the growth of P. amplifolius by 154% and 255%, respectively. Additionally, biomass was allocated differently depending on the resource: high light availability resulted in a higher root/shoot ratio, whereas high nutrient availability resulted in a lower root/shoot ratio. Low light availability and high nutrient availability increased the nitrogen content of leaf tissue by 53% and 40% respectively, resulting in a 37% and 31% decrease in the C/N ratio. Root nitrogen content was also increased by low light and high nutrient availability, by 50% (P=0.0807) and 77% respectively, resulting in a 20% and 40% decrease in root C/N ratio. Leaf phenolics were significantly increased 72% by high light and 31% by high nutrient availability, but root phenolic concentrations were not altered significantly. None of these changes in tissue constituents resulted in altered palatability to crayfish. N. advena was killed by the same high nutrient treatment that stimulated growth in P. amplifolius, preventing assessment of phenotypic responses to nutrient availability. However, high light availability increased overall growth by 24%, but this was mainly due to increased growth of the rhizome (increased 100%), resulting in a higher root/shoot ratio. High light tended to increase the production of floating leaves (P=0.09) and significantly decreased the production of submersed leaves. High light availability decreased the nitrogen content by 15% and 25% and increased the phenolic concentration by 88% and 255% in floating and submersed leaves, respectively. These differences in leaf traits did not result in detectable differences in damage by herbivores.


Nuphar Phenotypic plasticity Plant defenses Plant-herbivore interactions Potamogeton 



Funding for this project was provided by NSF DEB 94-08452 (to D.M. Lodge). We are grateful to Thomas and Patricia McCauslin for providing access to Gray Lake and the use of their boat and macrophyte wacker. Sarah Johnson devoted several hours to setting up and maintaining the field manipulations, Nate Dorn and Keith Bayha provided assistance, and Bill Perry provided the crayfish.


  1. Aliotta G, Molinario A, Monaco P, Pinto G, Previtera L (1992) Three biologically active phenylpropanoid glucosides from Myriophyllum verticillatum. Phytochemistry 31:109–111CrossRefGoogle Scholar
  2. Andersen RA, Todd JR (1968) Estimation of total tobacco phenols by their bonding to polyvinylpyrrolidone. Tob Sci 12:107–111Google Scholar
  3. Anderson MG (1978) Distribution and production of sago pondweed (Potamogeton pectinatus L.) on a northern prairie marsh. Ecology 59:154–160Google Scholar
  4. Barko JW, Smart RM (1986) Sediment-related mechanisms of growth limitation in submersed macrophytes. Ecology 67:1328–1340Google Scholar
  5. Bodkin PC, Spence DHN, Weeks DC (1980) Photoreversible control of heterophylly in Hippuris vulgaris L. New Phytol 84:533–542Google Scholar
  6. Bryant JP, Chapin FS, Klein DR (1983) Carbon/nutrient balance of boreal plants in relation to vertebrate herbivory. Oikos 40:357–368Google Scholar
  7. Bryant JP, Chapin FS, Reichardt PB, Clausen TP (1987) Response of winter chemical defense in Alaska paper birch and green alder to manipulation of plant carbon/nitrogen balance. Oecologia 72:510–514Google Scholar
  8. Carpenter SR, Lodge DM (1986) Effects of submersed macrophytes on ecosystem processes. Aquat Bot 26:341–370Google Scholar
  9. Coley PD, Aide TM (1991) Comparison of herbivory and plant defenses in temperate and tropical broad-leaved forests. In: Price PW, Lewinsohn TM, Fernandes GW, Benson WW (eds) Plant-animal interactions: evolutionary ecology in tropical and temperate region. Wiley, New York, pp 25–49Google Scholar
  10. Coley PD, Bryant JP, Chapin FS (1985) Resource availability and plant antiherbivore defense. Science 230:895–899Google Scholar
  11. Cronin G (1998) Influence of macrophyte structure, nutritive value, and chemistry on the feeding choices of a generalist crayfish. In: Jeppesen E, Sondergaard Ma, Sondergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes. Springer, Berlin Heidelberg New York, pp 307–317Google Scholar
  12. Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 325–353Google Scholar
  13. Cronin G, Hay ME (1996a) Effects of light and nutrient availability on the growth, secondary chemistry, and resistance to herbivory of two brown seaweeds. Oikos 77:93–106Google Scholar
  14. Cronin G, Hay ME (1996b) Seaweed-herbivore interactions depend on recent history of both the plant and animal. Ecology 77:1531–1543Google Scholar
  15. Cronin G, Schlacher T, Lodge DM, Siska EL (1999) Intraspecific variation in feeding preference and performance of Galerucella nymphaeae (Chrysomelidae: Coleoptera) on aquatic macrophytes. J N Am Benthol Soc 18:391–405Google Scholar
  16. Cronin G, Wissing KD, Lodge DM (1998) Comparative feeding selectivity of herbivorous insects on water lilies: aquatic vs. semi-terrestrial insects and submersed vs. floating leaves. Freshw Biol 39:243–257CrossRefGoogle Scholar
  17. Cronin G, Lodge DM, Hay ME, Miller M, Hill AM, Horvath T, Bolser RC, Lindquist N, Wahl M (2002) Crayfish feeding preferences for freshwater macrophytes: the influence of plant structure and chemistry. J Crustac Biol 22:708–718Google Scholar
  18. Damman H (1987) Leaf quality and enemy avoidance by the larvae of a pyralid moth. Ecology 68:88–97Google Scholar
  19. Denno RF, McClure MS (1983) Variable plants and herbivores in natural and managed systems. Academic Press, New YorkGoogle Scholar
  20. Denny P (1972) Sites of nutrient absorption in aquatic macrophytes. J Ecol 60:819–829Google Scholar
  21. Denny P (1980) Solute movement in submerged angiosperms. Biol Rev 55:65–92Google Scholar
  22. Dorn NJ, Cronin G, Lodge DM (2001) Feeding preferences and performance of an aquatic lepidopteran on macrophytes: plant hosts as food and habitat. Oecologia 128:406–415CrossRefGoogle Scholar
  23. Gallardo A, Merino J (1993) Leaf decomposition in two Mediterranean ecosystems of southwest Spain: influence of substrate quality. Ecology 74:152–161Google Scholar
  24. Givnish TJ (ed) (1986) On the economy of plant form and function. Cambridge University Press, New YorkGoogle Scholar
  25. Grime JP, Crick JC, Rincon JE (1986) The ecological significance of plasticity. In: Jennings DH, Trewavas AJ (eds) Plasticity in plants. The Company of Biologists, Cambridge, pp 5–29Google Scholar
  26. Gross EM, Sütfeld R (1994) Polyphenols with algicidal activity in the submerged macrophyte Myriophyllum spicatum L. Acta Hortic 381:710–716Google Scholar
  27. Gross EM, Meyer H, Schilling G (1996) Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry 41:133–138CrossRefGoogle Scholar
  28. Hagerman AE, Butler LG (1991) Tannins and lignins. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, vol 1. Chemical Participants Academic Press, New York, pp 355–388Google Scholar
  29. Herms DA, Mattson WJ (1992) The dilemma of plants: to grow or defend. Q Rev Biol 67:283–335Google Scholar
  30. Ikusima I (1970) Ecological studies on the productivity of aquatic plant communities: IV. Light conditions and community photosynthesis production. Bot Mag (Tokyo) 83:330–341Google Scholar
  31. Jeppesen E, Sondergaard Ma, Sondergaard Mo, Christoffersen K (eds) (1998) The structuring role of submerged macrophytes in lakes. Springer, Berlin Heidelberg New YorkGoogle Scholar
  32. Kouki J (1993) Herbivory modifies the production of different leaf types in the yellow water-lily, Nuphar lutea (Nymphaeaceae). Funct Ecol 7:21–26Google Scholar
  33. Lodge DM (1991) Herbivory on freshwater macrophytes. Aquat Botany 41:195–224Google Scholar
  34. Lodge DM, Cronin G, Van Donk E, Froelich AJ (1998) Impact of herbivory on plant standing crop: comparisons among biomes, between vascular and nonvascular plants, and among freshwater herbivore taxa. In: Jeppesen E, Sondergaard Ma, Sondergaard Mo, Christoffersen K (eds) The structuring role of submerged macrophytes in lakes, vol 131. Springer, Berlin Heidelberg New York, pp 149–174Google Scholar
  35. Loomis WE (1953a) Growth correlation. In: Loomis WE (ed) Growth and differentiation in plants: a monograph of the American Society of Plant Physiologists. Iowa State College Press, Ames, pp 197–217Google Scholar
  36. Loomis WE (1953b) Growth and differentiation: an introduction and summary. In: Loomis WE (ed) Growth and differentiation in plants: a monograph of the American Society of Plant Physiologists. Iowa State College Press, Ames, pp 1–17Google Scholar
  37. McClintock JB, Baker BJ (eds) (2001) Marine chemical ecology. CRC Press, Boca RatonGoogle Scholar
  38. Muzika RM (1993) Terpenes and phenolics in response to nitrogen fertilization: a test of the carbon/nutrient balance hypothesis. Chemoecology 4:3–7Google Scholar
  39. Newman RM (1991) Herbivory and detritivory on freshwater macrophytes by invertebrates: a review. J N Am Benthol Soc 10:89–114Google Scholar
  40. Newman RM, Hanscom Z, Kerfoot WC (1992) The watercress glucosinolate-myrosinase system: a feeding deterrent to caddisflies, snails, and amphipods. Oecologia 92:1–7Google Scholar
  41. Newman RM, Kerfoot WC, Hanscom Z (1996) Watercress allelochemical defends high-nitrogen foliage against consumption: effects on freshwater invertebrate herbivores. Ecology 77:2312–2323Google Scholar
  42. Perry WL, Lodge DM, Feder JL (2002) Importance of hybridization of indigenous and nonindigenous freshwater species: an overlooked threat to North American biodiversity. Syst Biol 51:255–275CrossRefPubMedGoogle Scholar
  43. Planas D, Sarhan F, Dube L, Godmaire H, Cadieux C (1981) Ecological significance of phenolic compounds of Myriophyllum spicatum. Verh Int Verein Limnol 21:1492–1496Google Scholar
  44. Puglisi MP, Paul VJ (1997) Intraspecific variation in the red alga Portieria hornemannii: monoterpene concentrations are not influenced by nitrogen or phosphorus enrichment. Mar Biol 128:161–170CrossRefGoogle Scholar
  45. Ragan MA, Glombitza KW (1986) Phlorotannins, brown algal polyphenols. In: Round FE, Chapman DJ (eds) Progress in phycological research, vol 4. Biopress, Bristol, pp 129–241Google Scholar
  46. Reichardt PB, Chapin FS, Bryant JP, Mattes BR, Clausen TP (1991) Carbon/nutrient balance as a predictor of plant defense in Alaskan balsam poplar: potential importance of metabolite turnover. Oecologia 88:401–406Google Scholar
  47. Rhoades DF (1983) Herbivore population dynamics and plant chemistry. In: Denno RF, McClure MS (eds) Variable plants and herbivores in natural and managed systems. Academic Press, New York, pp 155–220Google Scholar
  48. Rice WR, Gaines SD (1994) 'Heads I win, tails you lose': testing directional alternative hypotheses in ecological and evolutionary research. Trends Ecol Evol 9:235–237Google Scholar
  49. Rosenthal GA, Berenbaum MR (eds) (1992) Herbivores: their interactions with secondary plant metabolites, vol 2. Evolutionary and ecological processes. Academic Press, New YorkGoogle Scholar
  50. Saito K, Matsumoto M, Sekine T, Murakoshi I (1989) Inhibitory substances from Myriophyllum brasiliense on growth of blue-green algae. J Nat Prod 52:1221–1226Google Scholar
  51. Scheffer M, Hosper SH, Meijer ML, Moss B, Jeppesen E (1993) Alternative equilibria in shallow lakes. Trends Ecol Evol 8:275–279Google Scholar
  52. Solorzano L, Sharp J (1980) Determination of total dissolved phosphorus and particulate phosphorus in natural waters. Limnol Oceanogr 25:754–758Google Scholar
  53. Stout RJ (1989) Effects of condensed tannins on leaf processing in mid-latitude and tropical streams: a theoretical approach. Can J Fish Aquat Sci 46:1097–1106Google Scholar
  54. Titus JE (1996) Heterophylly in a water lily: interacting effects of [CO2] with sediment and water depth. Suppl Ecol Soc Am 77:443Google Scholar
  55. Tollrian R, Harvell CD (eds) (1999) The ecology and evolution of inducible defenses. Princeton University Press, New JerseyGoogle Scholar
  56. Tuomi J (1992) Toward integration of plant defence theories. Trends Ecol Evol 7:365–367Google Scholar
  57. Waterman PG, Mole S (1989) Extrinsic factors influencing the production of secondary metabolites in plants. In: Bernays EA (ed) Insect-plant interactions, vol 1. CRC, Boca Raton, pp 107–134Google Scholar
  58. White TCR (1969) An index to measure weather-induced stress of trees associated with outbreaks of psyllids in Australia. Ecology 50:905–909Google Scholar
  59. White TCR (1984) The abundance of invertebrate herbivores in relation to the availability of nitrogen in stressed food plants. Oecologia 63:90–105Google Scholar
  60. Wilson JB (1988) A review of evidence on the control of shoot:root ratio, in relation to models. Ann Bot 61:433–449Google Scholar
  61. Yates JL, Peckol P (1993) Effects of nutrient availability and herbivory on polyphenolics in the seaweed Fucus vesiculosus. Ecology 74:1757–1766Google Scholar
  62. Zangerl AR, Berenbaum MR (1987) Furanocoumarins in wild parsnip: effects of photosynthetically active radiation, ultraviolet light, and nutrients. Ecology 68:516–520Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Department of Biological SciencesUniversity of Notre DameNotre DameUSA
  2. 2.Department of BiologyUniversity of Colorado at DenverDenverUSA

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