The identification of a general connection between biogeochemistry and the structure of food webs would constitute a considerable advance in understanding ecosystems. Ecologists are on the case.
Organisms are the products of chemical reactions, and their growth depends on the availability of various elements, especially carbon, nitrogen and phosphorus. The growth-rate hypothesis1 links the relative element content of organisms to their growth rate, the idea being that fast-growing organisms need relatively more P-rich RNA, the main component of the protein-producing ribosome, to support rapid protein synthesis. Consequently, ecosystem conditions that produce organic matter with low C:P and N:P ratios would be expected to result in lower protein:RNA ratios, higher adaptive growth rates, more efficient energy transfer through a food web, and increased biomass of large-bodied animals relative to that of small-bodied animals1. In Global Change Biology, Mulder and Elser2 offer a first test of this association between C:N:P stoichiometry and faunal size spectrum for soil food webs.
Elser et al.3 had previously proposed the growth-rate hypothesis (GRH) to explain differences in C:N:P ratios among zooplankton species; support for the hypothesis in that context soon appeared4. Subsequent investigations5,6 revealed significant relationships between body C:N:P stoichiometry and growth rate in diverse groups of organisms. The scaling up of studies to the community level related the elemental stoichiometries of water environments and of body composition to the body-size spectrum of food webs in aquatic ecosystems7. But investigations of such relationships in terrestrial ecosystems are only now beginning8.
Mulder and Elser2 analysed the mass-abundance and body-size spectra of all soil invertebrates, fungi and bacteria in 22 grassland soils in the Netherlands. They find that the higher the availability of P in the soil (the lower the C:P ratio), the steeper is the slope of the faunal biomass size spectrum — that is, the biomass of large-bodied invertebrates becomes greater relative to that of small invertebrates. This relationship has broad implications because soil invertebrates of different sizes have different effects on soil processes. The relationship connects biogeochemistry with the structure of food webs, and — if it holds true in different settings — opens a way to developing more general laws of ecosystem structure and dynamics.
So Mulder and Elser's results2 are promising. Nonetheless, the association between soil-element stoichiometry and the body-size spectrum of the food web might not simply result from faster growth of different organisms in the food web in response to low C:P and protein:RNA ratios, as predicted by the GRH. As Mulder and Elser point out, other factors may be involved. For example, the shift in body-size spectrum might have resulted from the change from one main food resource (bacterial cells) to another (fungal remains) that Mulder and Elser found in their soils as C:P ratios decreased. The shift between these two different energy channels9, which differ in both productivity and turnover rate, could have driven the shift in invertebrate dominance from bacterium-feeding nematodes to microarthropods, which have different feeding habits and sizes. The link between C:P ratio and body-size spectrum could result from the microfauna (nematodes) coping better with P-limited conditions than the mesofauna (microarthropods).
Tests of the GRH are being extended to plants, which present a much more variable stoichiometry than animals or microbes10. In an investigation in pines just published in Ecology Letters, Matzek and Vitousek11 find no link between foliar N:P ratio and growth rate. In comparing leaves of the same species growing at different rates as a result of different nutrient conditions, they found that the faster-growing plants had lower protein:RNA ratios but not consistently lower N:P ratios; and in comparing several species with different growth rates, they found that there was no relation between growth rate and foliar N:P or protein:RNA ratios. Their results thus deviate from the predictions of the GRH.
Matzek and Vitousek11 conclude that plants adjust the balance of protein and RNA to favour either speed or efficiency of protein synthesis, depending on whether nutrient availability is high or low. According to this thinking, the balance of protein and RNA is not dictated only by the stoichiometry of elements in the leaf, nor does this balance, in isolation, dictate leaf N:P stoichiometry. In fact, the stoichiometry of plants might be decoupled from metabolic and physiological needs by storage of nutrients in vacuoles, obscuring the stoichiometric differences that would be expected given the protein:RNA ratios observed. Thus, the links between N:P stoichiometry and growth capacity in plants would seem not to be ruled by protein:RNA ratio alone.
Further assessment of the GRH evidently requires many more studies of the effects of C:N:P ratios on proteins and RNA, as well as on other different metabolic products, and on growth rates and body sizes in different taxa and ecosystems. The number of variables is bewildering, and, as is clear from these two papers2,11, the answers will not be universally straightforward.
Metabolomics analysis12 is emerging as one way forward, however. Improved analytical methods and computerized interpretation of large data sets have transformed the task of quantifying more metabolic compounds — carbohydrates, amino acids and peptides, lipids, phenolics, terpenoids, alkaloids and so on — and associating them with the corresponding elemental stoichiometries. Metabolomics should thus help to interpret the response of different groups of organisms in allocating resources to growth, storage and defence. It may also provide the elemental and metabolic budgets for different species along gradients from low to fast growth, which would allow a better test of the links between C:N:P ratio, growth rate and body-size spectrum.
This is an endeavour that goes well beyond assessment of the GRH. Such research will improve our understanding of the coupling between different levels of biological organization, from cellular metabolism to ecosystem structure and nutrient cycling. In doing so, it will help in integrating analysis of the pools and flows of chemical elements and energy studied in ecosystem ecology, with assessments of genetic fitness and the biochemical products of genomes considered in evolutionary ecology.
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Mulder, C. & Elser, J. J. Global Change Biol. 10.1111/j.1365-2486.2009.01899.x (2009).
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Gillooly, J. F., Charnov, E. L., West, G. B., Savage, V. M. & Brown, J. H. Nature 417, 70–73 (2002).
Niklas, K. J. Ann. Bot. 97, 155–163 (2006).
de Eyto, E. & Irvine, K. Ecosystems 17, 724–736 (2007).
Reuman, D. C., Cohen, J. E. & Mulder, C. Adv. Ecol. Res. 41, 45–85 (2009).
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