Advertisement

Oecologia

, Volume 174, Issue 4, pp 1367–1376 | Cite as

Differing nutritional constraints of consumers across ecosystems

  • Nathan P. Lemoine
  • Sean T. Giery
  • Deron E. Burkepile
Community ecology - Original research

Abstract

Stoichiometric mismatches between resources and consumers may drive a number of important ecological interactions, such as predation and herbivory. Such mismatches in nitrogen (N) or phosphorus (P) content between resources and consumers have furthered our understanding of consumer behavior and growth patterns in aquatic systems. However, stoichiometric data for multiple consumers from the same community are lacking in terrestrial systems. Here, we present the results of a study designed to characterize nutritional constraints within a terrestrial arthropod community. In order to place our results in a broader context, we compared our data on resource–consumer stoichiometry to those of stream and lake ecosystems. We found that N and P varied among trophic levels, and that high N:P content of herbivores suggests that herbivores might experience strong N-limitation. However, incredibly low P-content of plant foliage leads to potential P-limitation in herbivores that is nearly as strong as potential N-limitation. Moreover, arthropod predators may also be strongly P-limited. In fact, potential nutrient limitation of terrestrial herbivores in our study is similar to nutrient limitation from streams and lakes, suggesting that similar nutritional constraints may be operating across all three study systems. Importantly, our data suggest that consumers in lakes experience a trade-off between N- and P-limitation, while terrestrial consumers experience simultaneous strengthening or weakening of N- and P-limitation. We suggest that P may be overlooked as an important limiting nutrient in terrestrial ecosystems.

Keywords

Insects Diet Nitrogen Phosphorus Nutrient limitation Aquatic Stoichiometry 

Notes

Acknowledgments

We thank R. Decker for running our C:N:P nutrient analyses and C. Layman for feedback on previous drafts of the manuscript. This work was funded by a Presidential Fellowship for FIU (N.L.) and the College of Arts and Sciences at FIU (D.E.B.).

Supplementary material

442_2013_2860_MOESM1_ESM.docx (169 kb)
Supplementary material 1 (DOCX 169 kb)
442_2013_2860_MOESM2_ESM.pdf (456 kb)
Supplementary material 2 (PDF 455 kb)

References

  1. Allgeier JE, Rosemond AD, Layman CA (2011) The frequency and magnitude of non-additive responses to multiple nutrient enrichment. J Appl Ecol 48:96–101CrossRefGoogle Scholar
  2. Alves JM, Caliman A, Guariento RD, Figueiredo-Barros MP, Carniero LS, Farjalla VF, Bozelli RL, Esteves FA (2010) Stoichiometry of benthic invertebrate nutrient recycling: interspecific variation and the role of body mass. Aquatic Ecol 44:421–430CrossRefGoogle Scholar
  3. Back JA, Taylor JM, King RS, Fallert KL (2008) Ontogenetic differences in mayfly stoichiometry influence growth rates in response to phosphorus enrichment. Fund Appl Limnol 171:233–240CrossRefGoogle Scholar
  4. Bishop JG, O’Hara NB, Titus JH, Apple JL, Gill RA, Wynn L (2010) N-P co-limitation of primary production and response of arthropods to N and P in early primary succession on Mount St. Helens volcano. PloS ONE 5:e13598PubMedCentralPubMedCrossRefGoogle Scholar
  5. Burkepile DE (2013) Comparing aquatic and terrestrial grazing ecosystems: is the grass really greener? Oikos 122:306–312CrossRefGoogle Scholar
  6. Clissold FJ, Brown ZP, Simpson SJ (2013) Protein-induced mass increase of the gastrointestinal tract of locusts improves net nutrient uptake via larger meals rather than more efficient nutrient absorption. J Exp Biol 216:329–337PubMedCrossRefGoogle Scholar
  7. Cross WF, Benstead JP, Rosemond AD, Wallace JB (2003) Consumer-resource stoichiometry in detritus-based streams. Ecol Lett 6:721–732CrossRefGoogle Scholar
  8. Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531CrossRefGoogle Scholar
  9. Dobberfuhl DR, Elser JJ (2000) Elemental stoichiometry of lower food web components in arctic and temperate lakes. J Plankton Res 22:1341–1354CrossRefGoogle Scholar
  10. Elser JJ, Hassett RP (1994) A stoichiometric analysis of zooplankton-phytoplankton interactions in marine and freshwater ecosystems. Nature 370:211–213CrossRefGoogle Scholar
  11. Elser JJ, Fagan WF, Denno RF, Dobberfuhl DR, Folarin A, Huberty A, Interlandl S, Kilham SS, McCauley E, Schulz KL, Siemann EH, Sterner RW (2000) Nutritional constraints in terrestrial and freshwater food webs. Nature 408:578–580PubMedCrossRefGoogle Scholar
  12. Elser JJ, Acharya K, Kyle M, Cotner J, Makino W, Markow T, Watts T, Hobbie S, Fagan W, Schade J, Hood J, Sterner RW (2003) Growth-rate stoichiometry couplings in diverse biota. Ecol Lett 6:936–943CrossRefGoogle Scholar
  13. Elser JJ, Watts T, Bitler B, Markow TA (2006) Ontogenetic coupling of growth rate with RNA and P contents in five species of Drosophila. Funct Ecol 20:846–856CrossRefGoogle Scholar
  14. Elser JJ, Peace AL, Kyle M, Wojewodzic M, McCrackin ML, Andersen T, Hessen DO (2010) Atmospheric nitrogen deposition is associated with elevated phosphorus limitation of lake zooplankton. Ecol Lett 13:1256–1261PubMedCrossRefGoogle Scholar
  15. Fagan WF, Denno RF (2004) Stoichiometry of actual vs. potential predator-prey interactions: insights into nitrogen limitation for arthropod predators. Ecol Lett 7:876–883CrossRefGoogle Scholar
  16. Fagan WF, Siemann EH, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversification. Am Nat 160:784–802PubMedCrossRefGoogle Scholar
  17. González AL, Fariña JM, Kay AD, Pinto R, Marquet PA (2011) Exploring patterns and mechanisms of interspecific and intraspecific variation in body elemental composition of desert consumers. Oikos 120:1247–1255CrossRefGoogle Scholar
  18. Hambäck PA, Gilbert J, Schneider K, Martinson HM, Fagan WF (2009) Effects of body size, trophic mode and larval habitat on Diptera stoichiometry: a regional comparison. Oikos 118:615–623CrossRefGoogle Scholar
  19. Han W, Fang J, Guo D, Zhang Y (2005) Leaf nitrogen and phosphorus stoichiometry across 753 terrestrial plant species in China. New Phytol 168:377–385PubMedCrossRefGoogle Scholar
  20. Harpole WS, Ngai JT, Cleland EE, Seabloom EW, Borer ET, Bracken MES, Elser JJ, Gruner DS, Hillebrand H, Shurin JB, Smith JE (2011) Nutrient co-limitation of primary producer communities. Ecol Lett 14:852–862PubMedCrossRefGoogle Scholar
  21. Huberty AF, Denno RF (2006) Consequences of nitrogen and phosphorus limitation for the performance of two planthoppers with divergent life-history strategies. Oecologia 149:444–455PubMedCrossRefGoogle Scholar
  22. Jensen TC, Leinaas HP, Hessen DO (2006) Age-dependent shift in response to food elemental composition in Collembola: contrasting effects of dietary nitrogen. Oecologia 149:583–592PubMedCrossRefGoogle Scholar
  23. Joern A, Provin T, Behmer ST (2012) Not just the usual suspects: insect herbivore populations and communities are associated with multiple plant nutrients. Ecology 93:1002–1015PubMedCrossRefGoogle Scholar
  24. Karowe DN, Martin MM (1989) The effects of quantity and quality of diet nitrogen on the growth, efficiency of foot utilization, nitrogen budget, and metabolic rate of fifth-instar Spodoptera eridania larvae (Lepidoptera: Noctuidae). J Insect Physiol 35:699–708CrossRefGoogle Scholar
  25. Kinney KK, Lindroth RL, Jung SM, Nordheim EV (1997) Effects of CO2 and NO3-availability on deciduous trees: phytochemistry and insect performance. Ecology 78:215–230Google Scholar
  26. Malzahn A, Aberle N, Clemmesen C, Boersma M (2007) Nutrient limitation of primary producers affects planktivorous fish condition. Limnol Oceanogr 52:2062–2071CrossRefGoogle Scholar
  27. Martinson HM, Schneider K, Gilbert J, Hines JE, Hambäck PA, Fagan WF (2008) Detritivory: stoichiometry of a neglected trophic level. Ecol Res 23:487–491CrossRefGoogle Scholar
  28. Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161CrossRefGoogle Scholar
  29. Mayntz D, Raubenheimer D, Salomon M, Toft S, Simpson SJ (2005) Nutrient-specific foraging in invertebrate predators. Science 307:111–113PubMedCrossRefGoogle Scholar
  30. Moe SJ, Stelzer RS, Forman R, Harpole WS, Daufresne T, Yoshita T (2005) Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29–39CrossRefGoogle Scholar
  31. Niklas KJ, Owens T, Reich PB, Cobb ED (2005) Nitrogen/phosphorus leaf stoichiometry and the scaling of plant growth. Ecol Lett 8:636–642CrossRefGoogle Scholar
  32. Perkins MC, Woods HA, Harrison JF, Elser JJ (2004) Dietary phosphorus affects the growth of larval Manduca sexta. Arch Insect Biochem 55:153–168CrossRefGoogle Scholar
  33. Persson J, Fink P, Goto A, Hood JM, Jonas J, Kato S (2010) To be or not to be what you eat: regulation of stoichiometric homeostasis among autotrophs and heterotrophs. Oikos 119:741–751CrossRefGoogle Scholar
  34. Raubenheimer D, Simpson SJ (2003) Nutrient balancing in grasshoppers: behavioral and physiological correlates of diet breadth. J Exp Biol 206:1669–1681PubMedCrossRefGoogle Scholar
  35. Reich PB, Oleksyn J (2004) Global pattern of plant leaf N and P in relation to temperature and latitude. Proc Natl Acad Sci USA 101:11001–11006PubMedCentralPubMedCrossRefGoogle Scholar
  36. Rotjan RD, Idjadi JA (2013) Surf and turf: toward better synthesis by cross-system understanding. Oikos 122:285–287CrossRefGoogle Scholar
  37. Schade JD, Kyle M, Hobbie SE, Fagan WF, Elser JJ (2003) Stoichiometric tracking of soil nutrients by a desert herbivore. Ecol Lett 6:96–101CrossRefGoogle Scholar
  38. Sterner RW, Elser JJ (2002) Ecological stoichiometry: the biology of elements from molecules to the biosphere. Princeton University Press, Princtone, NJGoogle Scholar
  39. Tao L, Hunter MD (2012) Does anthropogenic nitrogen deposition induce phosphorus limitation in herbivore insects? Glob Change Biol 18:1843–1853CrossRefGoogle Scholar
  40. R Core Team (2012) R: a language and environment for statistical computing. Vienna, AustriaGoogle Scholar
  41. Vanni MJ, Flecker AS, Hood JM, Headworth JL (2002) Stoichiometry of nutrient recycling by vertebrates in a tropical stream: linking species identity and ecosystem processes. Ecol Lett 5:285–293CrossRefGoogle Scholar
  42. Visanuvimol L, Bertram SM (2011) How dietary phosphorus availability during development influences condition and life history traits of the cricket, Acheta domesticus. J Insect Sci 11:1–17CrossRefGoogle Scholar
  43. Williams RS, Lincoln DE, Thomas RB (1994) Loblolly pine grown under elevated CO2 affects early instar pine sawfly performance. Oecologia 98:64–71CrossRefGoogle Scholar
  44. Wolkovich EM, Regetz J, O’Connor MI (2012) Advances in global change research require open science by individual researchers. Glob Change Biol 18:2102–2110CrossRefGoogle Scholar
  45. Woods HA, Fagan WF, Elser JJ, Harrison JF (2004) Allometric and phylogenetic variation in insect phosphorus content. Funct Ecol 18:103–109CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Nathan P. Lemoine
    • 1
  • Sean T. Giery
    • 2
  • Deron E. Burkepile
    • 1
  1. 1.Department of BiologyFlorida International UniversityNorth MiamiUSA
  2. 2.Department of Applied EcologyNorth Carolina State UniversityRalieghUSA

Personalised recommendations