When microbes and consumers determine the limiting nutrient of autotrophs: A theoretical analysis

Proceedings of the Royal Society B: Biological Sciences

Volumn 276, Issue 1656, 2009, Pages 487-497

  Cherif, Mehdi ^a,b   Loreau, Michel ^b  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Detritivores; Ecological stoichiometry; Excess C cycling; Herbivory; Model; N:P ratio

Indexed keywords

ORGANIC CARBON;

AUTOTROPHY; CARBON CYCLE; FOOD WEB; GROWTH RESPONSE; HERBIVORY; NUTRIENT AVAILABILITY; NUTRIENT CYCLING; NUTRIENT LIMITATION; STOICHIOMETRY; THEORETICAL STUDY; TROPHIC LEVEL;

ARTICLE; AUTOTROPH; CONSUMER; DECOMPOSER; ENVIRONMENTAL MANAGEMENT; HERBIVORE; MICROORGANISM; OMNIVORE; PLANT; PLANT NUTRIENT; PRIORITY JOURNAL; STOICHIOMETRY; THEORETICAL MODEL;

EID: 58149107833     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2008.0560     Document Type: Article

References (61)

1. Ågren, G. I. 2004 The C : N : P stoichiometry of autotrophs - theory and observations. Ecol. Lett. 7, 185-191.
2. Andersen, T. & Hessen, D. O. 1991 Carbon, nitrogen, and phosphorus content of freshwater zooplankton. Limnol. Oceanogr. 36, 807-814.
3. Andersen, O. K., Goldman, J. C., Caron, D. A. & Dennett, M. R. 1986 Nutrient cycling in a microflagellate food chain: III. Phosphorus dynamics. Mar. Ecol. Prog. Ser. 31, 47-55.
4. Anderson, T. R., Hessen, D. O., Elser, J. J. & Urabe, J. 2005 Metabolic stoichiometry and the fate of excess carbon and nutrients in consumers. Am. Nat. 165, 1-15.
5. Arndt, H. 1993 Rotifers as predators on components of the microbial food web (bacteria, heterotrophic flagellates, ciliates) - a review. Hydrobiologia 255/256, 231-246.
6. Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyerreil, L. A. & Thingstad, F. 1983 The ecological role of water-column microbes in the sea. Mar. Ecol. Prog. Ser. 10, 257-263.
7. Ballantyne, F., Menge, D. N. L., Ostling, A. & Hosseini, P. 2008 Nutrient recycling affects autotroph and ecosystem stoichiometry. Am. Nat. 171, 511-523.
8. Banse, K. & Mosher, S. 1980 Adult body mass and annual production/biomass relationships of field populations. Ecol. Monogr. 50, 355-379.
9. Blackman, F. F. 1905 Optima and limiting factors. Ann. Bot. 19, 281-295.
10. Bratbak, G. & Thingstad, T. F. 1985 Phytoplankton-bacteria interactions: an apparent paradox? Analysis of a model system with both competition and commensalisms. Mar. Ecol. Prog. Ser. 25, 23-30.
11. Brendelberger, H. 1991 Filter mesh size of cladocerans predicts retention efficiency for bacteria. Limnol. Oceanogr. 36, 884-894.
12. Carlson, C. A. & Ducklow, H. W. 1996 Growth of bacterioplankton and consumption of dissolved organic carbon in the Sargasso Sea. Aquat. Microb. Ecol. 10, 69-85.
13. Carpenter, S. R., Cottingham, K. L. & Schindler, D. E. 1992 Biotic feedbacks in lake phosphorus cycles. Trends Ecol. Evol. 7, 332-336.
14. Cebrián, J. 1999 Patterns in the fate of production in plant communities. Am. Nat. 154, 449-468.
15. Cebrián, J. 2004 Role of first-order consumers in ecosystem carbon flow. Ecol. Lett. 7, 232-240.
16. Cleveland, C. C. & Liptzin, D. 2007 C : N : P stoichiometry in soil: is there a "Redfield ratio" for the microbial biomass? Biogeochemistry 85, 235-252.
17. Cotner, J. B., Makino, W. & Biddanda, B. A. 2006 Temperature affects stoichiometry and biochemical composition of Escherichia coli. Microb. Ecol. 52, 26-33.
18. Currie, D. J. & Kalff, J. 1984 A comparison of the abilities of freshwater algae and bacteria to acquire and retain phosphorus. Limnol. Oceanogr. 29, 298-310.
19. Curry, J. P. & Schmidt, O. 2007 The feeding ecology of earthworms - a review. Pedobiologia 50, 463-477.
20. Danger, M., Oumarou, C., Benest, D. & Lacroix, G. 2007 Bacteria can control stoichiometry and nutrient limitation of phytoplankton. Funct. Ecol. 21, 202-210.
21. Darchambeau, F., Faerovig, P. J. & Hessen, D. O. 2003 How Daphnia copes with excess carbon in its food. Oecologia 136, 336-346.
22. Daufresne, T. & Loreau, M. 2001a Plant-herbivore interactions and ecological stoichiometry: when do herbivores determine plant nutrient limitation? Ecol. Lett. 4, 196-206.
23. Daufresne, T. & Loreau, M. 2001b Ecological stoichiometry, primary producer-decomposer interactions, and ecosystem persistence. Ecology 82, 3069-3082.
24. Demoling, F., Figueroa, D. & Bååth, E. 2007 Comparison of factors limiting bacterial growth in different soils. Soil Biol. Biochem. 39, 2485-2495.
25. del Giorgio, P. A. & Cole, J. J. 1998 Bacterial growth efficiency in natural aquatic systems. Annu. Rev. Ecol. Syst. 29, 503-541.
26. Elser, J. J. & Urabe, J. 1999 The stoichiometry of consumer-driven nutrient recycling: theory, observations, and consequences. Ecology 80, 735-751.
27. Elser, J. J., Elser, M. M., Mackay, N. A. & Carpenter, S. R. 1988 Zooplankton-mediated transitions between N-limited and P-limited algal growth. Limnol. Oceanogr. 33, 1-14.
28. Elser, J. J. et al. 2000 Nutritional constraints in terrestrial and freshwater food webs. Nature 408, 578-580.
29. Elser, J. J. et al. 2007 Global analysis of nitrogen and phosphorus limitation of primary producers in freshwater, marine and terrestrial ecosystems. Ecol. Lett. 10, 1135-1142.
30. Frost, P. C., Cross, W. F. & Benstead, J. P. 2005 Ecological stoichiometry in freshwater benthic ecosystems: an introduction. Freshw. Biol. 50, 1781-1785.
31. Hassett, R. P., Cardinale, B., Stabler, L. B. & Elser, J. J. 1997 Ecological stoichiometry of N and P in pelagic ecosystems: comparison of lakes and oceans with emphasis on the zooplankton-phytoplankton interaction. Limnol. Oceanogr. 42, 648-662.
32. Hernández-León, S. & Ikeda, T. 2005 A global assessment of mesozooplankton respiration in the ocean. J. Plankt. Res. 27, 153-158.
33. Hunt, H. W., Coleman, D. C., Ingham, E. R., Ingham, R. E., Elliott, E. T., Moore, J. C., Rose, S. L., Reid, C. P. P. & Morley, C. R. 1987 The detrital food web in a shortgrass prairie. Biol. Fertil. Soils 3, 57-68.
34. Ilstedt, U. & Singh, S. 2005 Nitrogen and phosphorus limitations of microbial respiration in a tropical phosphorus-fixing acrisol (ultisol) compared with organic compost. Soil Biol. Biochem. 37, 1407-1410.
35. Jensen, T. C. & Hessen, D. O. 2007 Does excess dietary carbon affect respiration of Daphnia? Oecologia 152, 1432-1939.
36. Jumars, P. A., Penry, D. L., Baross, J. A., Perry, M. J. & Frost, B. W. 1989 Closing the microbial loop - dissolved carbon pathway to heterotrophic bacteria from incomplete ingestion, digestion and absorption in animals. Deep-Sea Res. 36, 483-495.
37. Kaye, J. P. & Hart, S. C. 1997 Competition for nitrogen between plants and soil microorganisms. Trends Ecol. Evol. 12, 139-142.
38. Lovett, G. M. & Ruesink, A. E. 1995 Carbon and nitrogen mineralization from decomposing gypsy moth frass. Oecologia 104, 133-138.
39. Makarewicz, J. C. & Likens, G. E. 1979 Structure and function of the zooplankton community of Mirror Lake, New Hampshire. Ecol. Monogr. 49, 109-127.
40. Makino, W. & Cotner, J. B. 2004 Elemental stoichiometry of a heterotrophic bacterial community in a freshwater lake: implication for growth- and resource-dependent variations. Aquat. Microb. Ecol. 34, 33-41.
41. Milton, Y. & Kaspari, M. 2007 Bottom-up and top-down regulation of decomposition in a tropical forest. Oecologia 153, 163-172.
42. Moore, J. C. et al. 2004 Detritus, trophic dynamics and biodiversity. Ecol. Lett. 7, 584-600.
43. Moore, J. C., McCann, K. & de Ruiter, P. C. 2005 Modeling trophic pathways, nutrient cycling, and dynamic stability in soils. Pedobiologia 49, 499-510.
44. Morita, R. Y. 1988 Bioavailability of energy and its relationship to growth and starvation survival in nature. Can. J. Microbiol. 34, 436-441.
45. Pirlot, S., Unrein, F., Descy, J. P. & Servais, P. 2007 Fate of heterotrophic bacteria in Lake Tamganyika (East Africa). FEMS Microbiol. Ecol. 62, 354-364.
46. Polis, G. A. & Strong, D. R. 1996 Food web complexity and community dynamics. Am. Nat. 147, 813-846.
47. Puccia, C. J. & Levins, R. 1986 Qualitative modeling of complex systems: an introduction to loop analysis and time averaging. Cambridge, MA: Harvard University Press.
48. Raynaud, X., Lata, J. C. & Leadley, P. W. 2006 Soil microbial loop and nutrient uptake by plants: a test using a coupled C : N model of plant-microbial interactions. Plant Soil 287, 95-116.
49. Rivkin, R. B. & Anderson, M. R. 1997 Inorganic nutrient limitation of oceanic bacterioplankton. Limnol. Oceanogr. 42, 730-740.
50. Rodríguez, H. & Fraga, R. 1999 Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol. Adv. 17, 319-339.
51. Rothhaupt, K. O. 1997 Grazing and nutrient influences of Daphnia and Eudiaptomus on phytoplankton in laboratory microcosms. J. Plankt. Res. 19, 125-139.
52. Schade, J. D., Kyle, M., Hobbie, S. E., Fagan, W. F. & Elser, J. J. 2003 Stoichiometric tracking of soil nutrients by a desert insect herbivore. Ecol. Lett. 6, 96-101.
53. Schroeder, L. A. 1981 Consumer growth efficiencies: their limits and relationships to ecological energetics. J. Theor. Biol. 93, 805-828.
54. Shurin, J. B., Gruner, D. S. & Hillebrand, H. 2006 All wet or dried up? Real differences between aquatic and terrestrial food webs. Proc. R. Soc. B 273, 1-9.
55. Stadler, B. & Müller, T. 1996 Aphid honeydew and its effect on the pyllosphere microflora of Picea abies (L.) Karst. Oecologia 108, 771-776.
56. Sterner, R. W. 1990 The ratio of nitrogen to phosphorus resupplied by herbivores: zooplankton and the algal competitive arena. Am. Nat. 136, 209-229.
57. Sterner, R. W., Elser, J. J. & Hessen, D. O. 1992 Stoichiometric relationships among producers, consumers and nutrient cycling in pelagic ecosystems. Biogeochemistry 17, 49-67.
58. Strom, S. L., Benner, R., Ziegler, S. & Dagg, M. J. 1997 Planktonic grazers are a potentially important source of marine dissolved organic carbon. Limnol. Oceanogr. 42, 1364-1374.
59. Tarafdar, J. C. & Claassen, N. 1988 Organic phosphorus compounds as a phosphorus source for higher plants through the activity of phosphatases produced by plant roots and microorganisms. Biol. Fertil. Soils 5, 308-312.
60. Tilman, D. 1980 Resources: a graphical-mechanistic approach to competition and predation. Am. Nat. 116, 362-393.
61. Tiunov, A. V. & Scheu, S. 2004 Carbon availability controls the growth of detritivores (Lumbricidae) and their effect on nitrogen mineralization. Oecologia 138, 83-90.