Hydrobiologia

, Volume 678, Issue 1, pp 155–165 | Cite as

Detritivores feeding on poor quality food are more sensitive to increased temperatures

  • Verónica Díaz Villanueva
  • Ricardo Albariño
  • Cristina Canhoto
Primary Research Paper

Abstract

As temperature increases the metabolic rates, the effect of warming on animals will also enhance animal-driven nutrient cycling with important consequences on ecosystem dynamics. We tested the effects of increased temperature (15 and 20°C, optimal and suboptimal temperatures, respectively) on metabolic rates of the shredder larvae Sericostoma vittatum fed on three diets, Alnus glutinosa (L.) Gaertn., Eucalyptus globulus Labill. and Quercus robur L. We measured P and N content in leaves, faeces and excreta and calculated C, N, and P assimilation efficiencies, and mass balances. Carbon assimilation efficiency (AE) was reduced at 20°C when larvae fed on Q. robur; nitrogen-AE was reduced at 20°C in all diets and phosphorus-AE was not affected by temperature. Larvae achieved a net N gain in all treatments, however, increased temperatures had a negative effect on N incorporation into body tissue. The mass balance of P was negatively affected by temperature; larvae fed on Q. robur and on E. globulus had null balances at 15°C and negative at 20°C. Our results showed that high temperature increased nutrient excretion and affected N:P ratios in excreta, thus changes in temperature may have severe consequences on larval mediated leaf litter processing and nutrient cycling. However, the type of diet seemed to modulate the way temperature affects larval metabolism regarding excretion rate and assimilation efficiencies. The extent to which optimal–suboptimal temperature variation will alter detritivore metabolism performance, internal nutrient balance and hence, cycling of elements in the environment seems crucial under global warming scenarios.

Keywords

Temperature Detritivores Ecological stoichiometry Nutrient cycling Streams 

Notes

Acknowledgments

We thank Ana R. Calapez for laboratory work and chemical determinations, and E. Balseiro and M.A.S. Graça for suggestions in a previous version of this manuscript. D. Howell kindly advised us with the factorial analysis of variance and provided the statistical program for use on R statistical package. This work was supported by a bi-national Visiting Grant (SECYT, Argentina and GRICES, Portugal: PO/PA05-BXV-015), the Portuguese Science Foundation (Project: PTDC/CLI/67180/2006) and IMAR (Portugal), and by the CONICET (Grant #PIP 112-200801-01702) and FONCYT (Grant #PICT-2007-01747) (Argentina).

References

  1. Abelho, M., 2001. From litterfall to breakdown in streams: a review. The Scientific World 1: 656–680.CrossRefGoogle Scholar
  2. Albariño, R. & E. Balseiro, 2001. Food quality, larval consumption and growth of Klapopteryx kuscheli (Plecoptera) from a South Andes stream. Journal of Freshwater Ecology 16: 517–526.CrossRefGoogle Scholar
  3. American Public Health Association (APHA), 1989. Standard methods for the examination of water, sewage, and wastewater. American Public Health Association, Washington, D.C.Google Scholar
  4. Anderson, T. R., M. Boersma & D. Raubenheimer, 2004. Stoichiometry: linking elements to biochemicals. Ecology 85: 1193–1202.CrossRefGoogle Scholar
  5. Bärlocher, F., 2005. A primer for statistical analysis. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to study litter decomposition. Springer, Dordrecht, The Netherlands: 297–304.Google Scholar
  6. Brown, J. H., J. F. Gilloly, A. P. Allen, V. M. Savage & G. B. West, 2004. Toward a metabolic theory of ecology. Ecology 85: 1771–1789.CrossRefGoogle Scholar
  7. Canhoto, C. & M. A. S. Graça, 1995. Food value of introduced eucalypt leaves for a Mediterranean stream detritivore: Tipula lateralis. Freshwater Biology 34: 209–214.CrossRefGoogle Scholar
  8. Canhoto, C., F. Bärlocher & M. A. S. Graça, 2002. The effects of Eucalyptus globulus oils on fungal enzymatic activity. Archiv für Hydrobiologie 154: 121–132.Google Scholar
  9. Canhoto, C., M. A. S. Graça & F. Bärlocher, 2005. Feeding preferences of shredders. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to study litter decomposition. Springer, Dordrecht, The Netherlands: 297–304.CrossRefGoogle Scholar
  10. Coleman, D. C., C. P. P. Reid & C. V. Cole, 1983. Biological strategies of nutrient cycling in soil systems. Advances in Ecological Research 13: 1–55.CrossRefGoogle Scholar
  11. Cross, W. F., J. P. Benstead, A. D. Rosemond & J. B. Wallace, 2003. Consumer-resource stoichiometry in detritus-based streams. Ecology Letters 6: 721–732.CrossRefGoogle Scholar
  12. Darchambeau, F., P. J. Faerøvig & D. O. Hessen, 2003. How Daphnia copes with excess carbon in its food. Oecologia 136: 336–346.PubMedCrossRefGoogle Scholar
  13. Devine, J. A. & M. J. Vanni, 2002. Spatial and seasonal variation in nutrient excretion by benthic invertebrates in a eutrophic reservoir. Freshwater Biology 47: 1107–1121.CrossRefGoogle Scholar
  14. Dodds, W. K., V. H. Smith & K. Lohman, 2002. Nitrogen and phosphorus relationships to benthic algal biomass in temperate streams. Canadian Journal of Fisheries and Aquatic Science 59: 865–874.CrossRefGoogle Scholar
  15. Elser, J. J., W. F. Fagan, R. F. Denno, D. R. Dobberfuhl, A. Folarin, A. Huberty, S. Interlandi, S. S. Kilham, E. McCauleyk, K. L. Schulz, E. H. Siemann & R. W. Sterner, 2000. Nutritional constraints in terrestrial and freshwater foodwebs. Nature 408: 578–580.PubMedCrossRefGoogle Scholar
  16. Feio, M. J. & M. A. S. Graça, 2000. Food consumption by the larvae of Sericostoma vittatum (Trichoptera), an endemic species from the Iberian Peninsula. Hydrobiologia 439: 7–11.CrossRefGoogle Scholar
  17. Fenchel, T., 1988. Marine plankton food chains. Annual Review of Ecology and Systematics 19: 19–38.CrossRefGoogle Scholar
  18. Flindt, M. R. & A. I. Lillebo, 2005. Determination of total nitrogen and phosphorus in leaf litter. In Graça, M. A. S., F. Bärlocher & M. O. Gessner (eds), Methods to study litter decomposition. Springer, Dordrecht, The Netherlands: 53–60.CrossRefGoogle Scholar
  19. Friberg, N. & D. Jacobsen, 1999. Variation in growth of the detritivore-shredder Sericostoma personatum (Trichoptera). Freshwater Biology 42: 625–635.CrossRefGoogle Scholar
  20. Frost, P. C., R. S. Stelzer, G. A. Lamberti & J. J. Elser, 2002. Ecological stoichiometry of trophic interactions in the benthos: understanding the role of C:N:P ratios in lentic and lotic habitats. Journal of the North American Benthological Society 21: 515–528.CrossRefGoogle Scholar
  21. Frost, P. C., M. A. Evans-White, Z. V. Finkel, T. C. Jensen & V. Matzek, 2005. Are you what you eat? Physiological constraints on organismal stoichiometry in an elementally imbalanced world. Oikos 109: 18–28.CrossRefGoogle Scholar
  22. González, J. M. & M. A. S. Graça, 2003. Conversion of leaf litter to secondary production by a shredding caddis-fly. Freshwater Biology 48: 1578–1592.CrossRefGoogle Scholar
  23. Hladyz, S., M. O. Gessner, P. S. Giller, J. Pozo & G. Woodward, 2009. Resource quality and stoichiometric constraints on stream ecosystem functioning. Freshwater Biology 54: 957–970.CrossRefGoogle Scholar
  24. Houghton, J. T., Y. Ding, D. J. Griggs, M. Noguer, P. J. van der Linden, X. Dai, K. Maskell & C. A. Johnson, 2001. Climate Change 2001: The Scientific Basis. Cambridge University Press, Cambridge, UK.Google Scholar
  25. Intergovernmental Panel on Climate Change (IPCC), 2007. Climate change 2007: the physical science basis. In Solomon, S., D. Qin, M. Manning, Z. Chen, M. Marquis, K. B. Averyt, M. Tignor & H. L. Miller (eds), IPCC Fourth Assessment Report. IPCC, Geneva, Switzerland.Google Scholar
  26. Iversen, T. M., 1974. Ingestion and growth in Sericostoma personatum (Trichoptera) in relation to the nitrogen content of ingested leaves. Oikos 25: 278–282.CrossRefGoogle Scholar
  27. Lawton, J. H. & J. Richards, 1970. Comparability of Cartesian Diver, Gilson, Warburg and Winkler methods of measuring the respiratory rates of aquatic invertebrates in ecological studies. Oecologia 4: 319–324.CrossRefGoogle Scholar
  28. Lee, K. P., 2007. The interactive effects of protein quality and macronutrient imbalance on nutrient balancing in an insect herbivore. The Journal of Experimental Biology 210: 3236–3244.PubMedCrossRefGoogle Scholar
  29. Liess, A. & H. Hillebrand, 2006. Role of nutrient supply in grazer–periphyton interactions: reciprocal influences of periphyton and grazer nutrient stoichiometry. Journal of the North American Benthological Society 25: 632–642.CrossRefGoogle Scholar
  30. McManamay, R. A., J. R. Webster, H. M. Valett & C. A. Dolloff, 2011. Does diet influence consumer nutrient cycling? Macroinvertebrate and fish excretion in streams. Journal of the North American Benthological Society 30: 84–102.CrossRefGoogle Scholar
  31. Mulholland, P. J., 1996. Role in nutrient cycling in streams. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, CA: 609–640.Google Scholar
  32. Parmesan, C. & G. Yohe, 2003. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421: 37–42.PubMedCrossRefGoogle Scholar
  33. Quinn, G. & M. Keough, 2002. Experimental Design and Data Analysis for Biologist. Cambridge University Press, Cambridge, UK.Google Scholar
  34. R Development Core Team, 2010. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0.Google Scholar
  35. Rothlisberger, J. D., M. A. Baker & P. C. Frost, 2008. Effects of periphyton stoichiometry on mayfly excretion rates and nutrient ratios. Journal of the North American Benthological Society 27: 497–508.CrossRefGoogle Scholar
  36. Savage, V. M., J. F. Gillooly, J. H. Brown, G. B. West & E. L. Charnov, 2004. Effects of body size and temperature on population growth. The American Naturalist 163: 429–441.PubMedCrossRefGoogle Scholar
  37. Scriber, J. M. & F. Slansky, 1981. The nutritional ecology of immature insects. Annual Review of Entomology 26: 183–211.CrossRefGoogle Scholar
  38. Small, G. E. & C. M. Pringle, 2010. Deviation from strict homeostasis across multiple trophic levels in an invertebrate consumer assemblage exposed to high chronic phosphorus enrichment in a Neotropical stream. Oecologia 162: 581–590.PubMedCrossRefGoogle Scholar
  39. Steinman, A. D. 1996. Effects of grazers on freshwater benthic algae. In Stevenson, R. J., M. L. Bothwell & R. L. Lowe (eds), Algal Ecology: Freshwater Benthic Ecosystems. Academic Press, San Diego, CA: 341–374.Google Scholar
  40. Sterner, R. W. & J. J. Elser, 2002. Ecological stoichiometry. The biology of elements from molecules to the biosphere. Princeton University Press, Princeton, NJ.Google Scholar
  41. Tank, J. L., J. L. Meyer, D. M. Sanzone, P. J. Mulholland, J. R. Webster, B. J. Peterson, W. M. Wollheim & N. E. Leonard, 2000. Analysis of nitrogen cycling in a forest stream during autumn using a N-15-tracer addition. Limnology and Oceanography 45: 1013–1029.CrossRefGoogle Scholar
  42. Vanni, M. J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33: 341–370.CrossRefGoogle Scholar
  43. Walther, G. R., E. Post, P. Convey, A. Menzel, C. Parmesank, T. J. C. Beebee, J.-M. Fromentin, O. Hoegh-Guldberg & F. Bairlein, 2002. Ecological responses to recent climate change. Nature 416: 389–395.PubMedCrossRefGoogle Scholar
  44. Ward, J. V. & J. A. Stanford, 1982. Thermal responses in the evolutionary ecology of aquatic insects. Annual Review of Entomology 27: 97–117.CrossRefGoogle Scholar
  45. Winkler, L. W., 1888. Die Bestimmung des in Wasser gelösten Sauerstoffen. Berichte der Deutschen Chemischen Gesellschaft 21: 2843–2855.CrossRefGoogle Scholar
  46. Woods, H. A., W. Makino, J. B. Cotner, S. E. Hobbie, J. F. Harrison, K. Acharya & J. J. Elser, 2003. Temperature and the chemical composition of poikilothermic organisms. Functional Ecology 17: 237–245.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  • Verónica Díaz Villanueva
    • 1
  • Ricardo Albariño
    • 1
  • Cristina Canhoto
    • 2
  1. 1.Laboratorio de Limnologia-INIBIOMAUniversidad Nacional del ComahueBarilocheArgentina
  2. 2.IMAR & Department of ZoologyUniversity of CoimbraCoimbraPortugal

Personalised recommendations