Sex and size matter: Ontogenetic patterns of nutrient content of aquatic insects

Freshwater Science

Volumn 32, Issue 3, 2013, Pages 837-848

  Back, Jeffrey A ^a   King, Ryan S ^a  

^a BAYLOR UNIVERSITY   (United States)

Author keywords

aquatic insects; ecological stoichiometry; elemental composition; homeostasis; nutrient patterns; ontogeny; phosphorus

Indexed keywords

AQUATIC ORGANISM; BIOCHEMICAL COMPOSITION; BODY SIZE; ENTOMOLOGY; FLY; GROWTH RATE; HOMEOSTASIS; LARVA; LIFE HISTORY TRAIT; NUTRIENT AVAILABILITY; ONTOGENY; PHOSPHORUS; STOICHIOMETRY;

AMBRYSUS CIRCUMCINCTUS; EPHEMEROPTERA; HEXAPODA; LEPTOPHLEBIIDAE;

EID: 84884338991     PISSN: 21619549     EISSN: 21619565     Source Type: Journal    
DOI: 10.1899/12-181.1     Document Type: Article

References (64)

1. ACHARYA, K., M. KYLE, AND J. J. ELSER. 2004. Biological stoichiometry of Daphnia growth: an ecophysiological test of the growth rate hypothesis. Limnology and Oceanography 49:656-665.
2. ANDERSEN, T., J. J. ELSER, AND D. O. HESSEN. 2004. Stoichiometry and population dynamics. Ecology Letters 7: 884-900.
3. ANDERSEN, T., AND D. O. HESSEN. 1991. Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnology and Oceanography 36:807-814.
4. ARENDT, J. D. 1997. Adaptive intrinsic growth rates: an integration across taxa. Quarterly Review of Biology 72: 149-177.
5. BACK, J. A., J. M. TAYLOR, R. S. KING, K. L. FALLERT, AND E. H. HINTZEN. 2008. Ontogenic differences in mayfly stoichiometry influence growth rates in response to phosphorus enrichment. Fundamental and Applied Limnology 171:233-240.
6. BOGGS, C. L. 1990. A general model of the role of maledonated nutrients in female insects' reproduction. American Naturalist 136:598-617.
7. BOGGS, C. L., AND L. E. GILBERT. 1979. Male contribution to egg production in butterflies: evidence for transfer of nutrients at mating. Science 206:83-84.
8. BONNER, J. T. 1965. Size and cycle: an essay on the structure of biology. Princeton University Press, Princeton, New Jersey.
9. BOWMAN, M. F., P. A. CHAMBERS, AND D. W. SCHINDLER. 2005. Changes in stoichiometric constraints on epilithon and benthic macroinvertebrates in response to slight nutrient enrichment of mountain rivers. Freshwater Biology 50:1836-1852.
10. BRITTAIN, J. E. 1982. Biology of mayflies. Annual Review of Entomology 27:119-147.
11. BROWN, H. P. 1987. Biology of riffle beetles. Annual Review of Entomology 32:253-273.
12. CROSS, W. F., J. P. BENSTEAD, A. D. ROSEMOND, AND J. B. WALLACE. 2003. Consumer-resource stoichiometry in a detritus-based stream. Ecology Letters 6:721-732.
13. CROSS, W. F., B. R. JOHNSON, J. B. WALLACE, AND A. D. ROSEMOND. 2005. Contrasting response of stream detritivores to long-term nutrient enrichment. Limnology and Oceanography 50:1730-1739.
14. EDMUNDS, G. F., S. L. JENSEN, AND L. BERNER. 1976. The mayflies of north and central America. University of Minnesota Press, Minneapolis, Minnesota.
15. ELSER, J. J., K. ACHARYA, M. KYLE, J. COTNER, W. MANKINO, T. MARKOW, T. WATTS, S. HOBBIE, W. FAGAN, J. SCHADE, J. HOOD, AND R. W. STERNER. 2003. Growth rate-stoichiometry couplings in diverse biota. Ecology Letters 6:936-943.
16. ELSER, J. J., D. R. DOBBERFUHL, N. A. MACKAY, AND J. H. SCHAMPEL. 1996. Organism size, life history, and N:P stoichiometry: toward a unified view of cellular and ecosystem processes. BioScience 46:674-684.
17. ELSER, J. J., R. W. STERNER, A. E. GALFORD, T. H. CHRZANOWSKI, D. L. FINDLAY, K. H. MILLS, M. J. PATERSON, M. P. STAINTON, AND D. W. SCHINDLER. 2000. Pelagic C:N:P stoichiometry in a eutrophied lake: responses to a whole-lake food-web manipulation. Ecosystems 3: 293-307.
18. ELSER, J. J., AND J. URABE. 1999. The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80:735-751.
19. ELSER, J. J., T. WATTS, B. BITLER, AND T. A. MARKOW. 2006. Ontogenetic coupling of growth rate with RNA and P content in five species of Drosophila. Functional Ecology 20:846-856.
20. ENGQVIST, L. 2005. The mistreatment of covariate interaction terms in linear model analyses of behavioural and evolutionary ecology studies. Animal Behaviour 70: 967-971.
21. EVANS-WHITE, M. A., AND G. A. LAMBERTI. 2006. Stoichiometry of consumer-driven nutrient recycling across nutrient regimes in streams. Ecology Letters 9:1186-1197.
22. EVANS-WHITE, M. A., R. S. STELZER, AND G. A. LAMBERTI. 2005. Taxonomic and regional patterns in benthic macroinvertebrate elemental composition in streams. Freshwater Biology 50:1786-1799.
23. FÆRØVIG, P. J., AND D. O. HESSEN. 2003. Allocation strategies in crustacean stoichiometry: the potential role of phosphorus in the limitation of reproduction. Freshwater Biology 48:1782-1792.
24. FAGAN, W. F., E. SIEMANN, C. MITTER, R. F. DENNO, A. F. HUBERTY, H. A. WOODS, AND J. J. ELSER. 2002. Nitrogen in insects: implications for trophic complexity and species diversification. American Naturalist 160:784-802.
25. FOX, J., AND S. WEISBERG. 2011. An R companion to applied regression. 2nd edition. Sage, Thousand Oaks, California.
26. FROST, P. C., AND J. J. ELSER. 2002. Growth response of littoral mayflies to the phosphorus content of their food. Ecology Letters 5:232-240.
27. FROST, P. C., S. E. TANK, M. A. TURNER, AND J. J. ELSER. 2003. Elemental composition of littoral invertebrates from oligotrophic and eutrophic Canadian lakes. Journal of the North American Benthological Society 22:51-62.
28. GRIFFITH, G. E., S. A. BRYCE, J. M. OMERNIK, J. A. COMSTOCK, A. C. ROGERS, B.HARRISON, S. L.HATCH, AND D. BEZANSON. 2004. Ecoregions of Texas (color poster with map, descriptive text, and photographs). US Geological Survey, Reston, Virginia.
29. HAMBÄ CK, P. A., J. GILBERT, K. SCHNEIDER, H. M. MARTINSON, G. KOLB, AND W. F. FAGAN. 2009. Effects of body size, trophic mode and larval habit on Diptera stoichiometry: a regional comparison. Oikos 118:615-623.
30. HESSEN, D. O., AND A. LYNCH. 1991. Inter-and intraspecific variations in zooplankton element composition. Archiv fü r Hydrobiologie 121:355-363.
31. KAHLERT, M. 1998. C:N:P ratios of freshwater benthic algae. Archiv fü r Hydrobiologie Special Issues: Ergebnisse der Limnologie, Advances in Limnology 51:105-114.
32. KING, R. S., B. W. BROOKS, J. A. BACK, J.M. TAYLOR, AND B. A. FULTON. 2009. Linking observational and experimental approaches for the development of regional nutrient criteria for wadeable streams. CP-966137-01. Region 6. US Environmental Protection Agency, Dallas, TX.
33. KING, R. S., AND C. J. RICHARDSON. 2007. Subsidy-stress response of macroinvertebrate community biomass to a phosphorus gradient in an oligotrophic wetland ecosystem. Journal of the North American Benthological Society 26:169-184.
34. LAURIDSEN, R. B., F. K. EDWARDS, M. J. BOWES, G. WOODWARD, A. G. HILDREW, A. T. IBBOTSON, AND J. I. JONES. 2012. Consumer-resource elemental imbalances in a nutrientrich stream. Freshwater Science 31:408-422.
35. LIESS, A., AND H. HILLEBRAND. 2005. Stoichiometric variation in C:N, C:P, and N:P ratios of littoral benthic invertebrates. Journal of the North American Benthological Society 24:256-269.
36. MAIN, T. M., D. R. DOBBERFUHL, AND J. J. ELSER. 1997. N:P stoichiometry and ontogeny of crustacean zooplankton: a test of the growth rate hypothesis. Limnology and Oceanography 42:1474-1478.
37. MARKOW, T. A., A. COPPOLA, AND T. D. WATTS. 2001. How Drosophila males make eggs: it is elemental. Proceedings of the Royal Society of London Series B: Biological Sciences 268:1527-1532.
38. MARKOW, T. A., B. RAPHAEL, D. DOBBERFUHL, C.M. BREITMEYER, J. J. ELSER, AND E. PFEILER. 1999. Elemental stoichiometry of Drosophila and their hosts. Functional Ecology 13: 78-84.
39. MILTNER, R. J., AND E. T. RANKIN. 1998. Primary nutrients and the biotic integrity of rivers and streams. Freshwater Biology 40:145-158.
40. MOE, S. J., R. S. STELZER, M. R. FOREMAN, J. S. HARPOLE, T. DAUFRESNE, AND T. YOSHIDA. 2005. Recent advances in ecological stoichiometry: insights for population and community ecology. Oikos 109:29-39.
41. MOREHOUSE, N. I., T. NAKAZAWA, C. M. BOOHER, P. D. JEYASINGH, AND M. D. HALL. 2010. Sex in a material world: why the study of sexual reproduction and sex-specific traits should become more nutritionally-explicit. Oikos 119:766-778.
42. OGDEN, T. H., J. L. GATTOLLIAT, M. SARTORI, A. H. STANICZEK, T. SOLDÁ N, AND M. F. WHITING. 2009. Towards a new paradigm in mayfly phylogeny (Ephemeroptera): combined analysis of morphological and molecular data. Systematic Entomology 34:616-634.
43. PETERS, R. H. 1983. The ecological implications of body size. Cambridge University Press, Cambridge, UK.
44. RAMOS, I., F. GOMES, C. M. KOELLER, K. SAITO, N. HEISE, H. MASUDA, R. DOCAMPO, W. DE SOUZA, E. A. MACHADO, AND K. MIRANDA. 2011. Acidocalcisomes as calcium-and polyphosphate-storage compartments during embryogenesis of the insect Rhodnius prolixus Stahl. PLoS ONE 6(11):e27276.
45. RAPOPORT, S., AND G. M. GUEST. 1941. Distribution of acidsoluble phosphorus in the blood cells of various vertebrates. Journal of Biological Chemistry 138: 269-282.
46. ROONEY, J., AND S. M. LEWIS. 1999. Differential allocation of male-derived nutrients in two lampyrid beetles with contrasting life-history characteristics. Behavioral Ecology 10:97-104.
47. ROTHLISBERGER, J. D., M. A. BAKER, AND 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.
48. SHURIN, J. B., D. S. GRUNER, AND H. HILLEBRAND. 2006. All wet or dried up. Real differences between aquatic and terrestrial food webs. Proceedings of the Royal Society of London Series B: Biological Sciences 273:1-9.
49. SMALL, G. E., AND 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 (Berlin) 162:581-590.
50. STERNER, R. W., AND J. J. ELSER. 2002. Ecological stoichiometry. Princeton University Press, Princeton, New Jersey.
51. STERNER, R. W., AND D. O. HESSEN. 1994. Algal nutrient limitation and the nutrition of aquatic herbivores. Annual Review of Ecology and Systematics 25:1-29.
52. TAYLOR, J. M., AND J. H. KENNEDY. 2006. Life history and secondary production of Caenis latipennis (Ephemeroptera: Caenidae) in Honey Creek, Oklahoma. Annals of the Entomological Society of America 99:821-830.
53. URABE, J., J. CLASEN, AND R. W. STERNER. 1997. Phosphoruslimitation of Daphnia growth: Is it real? Limnology and Oceanography 42:1436-1443.
54. VANNI, M. J., A. S. FLECKER, J.M. HOOD, AND J. L. HEADWORTH. 2002. Stoichiometry of nutrient recycling by vertebrates in a tropical stream: Linking biodiversity and ecosystem function. Ecology Letters 5:285-293.
55. VELDBOOM, J. A., AND R. J. HARO. 2011. Stoichiometric relationship between suspension-feeding caddisfly (Trichoptera: Brachycentridae) and seston. Hydrobiologia 675:129-141.
56. VILLAR-ARGAIZ, M., J. M. MEDINA-SÁ NCHEZ, AND P. CARRILLO. 2002. Linking life history strategies and ontogeny in crustacean zooplankton: Implications for homeostasis. Ecology 83:1899-1914.
57. VILLAR-ARGAIZ, M., AND R. W. STERNER. 2002. Life history bottlenecks in Diaptomus clavipes induced by phosphoruslimited algae. Limnology and Oceanography 47:1229-1233.
58. VREDE, T., T. ANDERSEN, AND D. O. HESSEN. 1999. Phosphorus distribution in three crustacean zooplankton species. Limnology and Oceanography 44:225-229.
59. VREDE, T., D. R. DOBBERFUHL, S. A. L. KOOIJMAN, AND J. J. ELSER. 2004. Fundamental connections among organism C:N:P stoichiometry, macromolecular composition, and growth. Ecology 85:1217-1229.
60. WAGENHOFF, A., C. R. TOWNSEND, N. PHILLIPS, AND C. D. MATTHAEI. 2011. Subsidy-stress and multiple-stressor effects along gradients of deposited fine sediment and dissolved nutrients in a regional set of streams and rivers. Freshwater Biology 56:1916-1936.
61. WEIDER, L. J., J. J. ELSER, T. J. CREASE, M. MATEOS, J. B. COTNER, AND T. A. MARKOW. 2005. The functional significance of ribosomal (r)DNA variation: impacts on evolutionary ecology of organisms. Annual Review of Ecology and Systematics 36:219-242.
62. WHITE, D. S. 1978. Life cycle of the riffle beetle Stenelmis sexlineata (Elmidae). Annals of the Entomological Society of America 71:121-125.
63. WOODS, H. A., W. F. FAGAN, J. J. ELSER, AND J. F. HARRISON. 2004. Allometric and phylogenetic variation in insect phosphorus content. Functional Ecology 18:103-109.
64. ZEH, D. W., AND R. L. SMITH. 1985. Paternal investment by terrestrial arthropods. American Zoologist 25:785-805.