Linking the global carbon cycle to individual metabolism

Abstract

Summary1. We present a model that yields ecosystem-level predictions of the flux, storage and turnover of carbon in three important pools (autotrophs, decomposers, labile soil C) based on the constraints of body size and temperature on individual metabolic rate. 2. The model predicts a 10 000-fold increase in C turnover rates moving from tree-to phytoplankton-dominated ecosystems due to the size dependence of photosynthetic rates. 3. The model predicts a 16-fold increase in rates controlled by respiration (e.g. decomposition, turnover of labile soil C and microbial biomass) over the temperature range 0-30 °C due to the temperature dependence of ATP synthesis in respiratory complexes. 4. The model predicts only a fourfold increase in rates controlled by photosynthesis (e.g. net primary production, litter fall, fine root turnover) over the temperature range 0-30 °C due to the temperature dependence of Rubisco carboxylation in chloroplasts. 5. The difference between the temperature dependence of respiration and photosynthesis yields quantitative predictions for distinct phenomena that include acclimation of plant respiration, geographic gradients in labile C storage, and differences between the short-and long-term temperature dependence of whole-ecosystem CO 2 flux. 6. These four sets of model predictions were tested using global compilations of data on C flux, storage and turnover in ecosystems. 7. Results support the hypothesis that the combined effects of body size and temperature on individual metabolic rate impose important constraints on the global C cycle. The model thus provides a synthetic, mechanistic framework for linking global biogeochemical cycles to cellular-, individual-and community-level processes.

Metabolic theory predicts whole-ecosystem properties

“…These data have been temperature corrected to 15°C and include a large diversity of tissue types (Materials and Methods and SI Appendix, Table S2). As we also predict, in entire ecosystems, carbon residence times increase with (B) increasing body size of the primary producers (slope is 0.21 ± 0.02 95% CI; expected slope is <0.25 depending on the network, see prediction 3 in main text), data replotted from Allen et al (10), and (C) the ratio of total biomass to primary production (slope is 0. forests with agricultural fields and grasslands (39)(40)(41)(42), and a warmer climate, which increases metabolic rates, should decrease the residence time of carbon in local ecosystems and in the biosphere as a whole. More generally, our theory is a synthesis of systems and metabolic approaches that shows explicitly and quantitatively how organisms control the carbon cycle at all scales from individuals to ecosystems to the biosphere.…”

“…4A). The dependence of residence time in ecosystems on the body sizes of primary producers was assessed using a large existing dataset (10). As predicted, the observed α = 0.21 was somewhat less than 1/4 (Fig.…”

“…Our theory extends the bottom-up individual-based framework of metabolic theory (10,17,35) to ecosystems to incorporate organisms and their metabolism explicitly into ecological systems theory (15,16,20,21,31). It reveals how the size and temperature of the plants, animals, and microbes in different trophic compartments affect carbon residence time, and other emergent ecosystem properties such as TST and recycling (FCI).…”

“…From a large dataset compiled by Cebrian et al (12), we obtained the relevant data for 46 ecosystems representing a variety of habitats (terrestrial and marine), environmental temperatures (temperate to tropical), and organism body sizes (phytoplankton to trees and whales). The predicted dependence of ecosystem residence time on the body sizes of primary producers was evaluated using a different but overlapping dataset (10).…”

“…Although it has long been recognized that different kinds of organisms play important roles in the processing of energy and materials in ecosystems, existing treatments are incomplete. Most studies have focused on particular trophic levels, such as primary producers or herbivores, specific ecosystem types, such as tropical forest or pelagic marine, or single species, such as top predators or ecosystem engineers (4)(5)(6)(7)(8)(9)(10)(11)(12)(13)(14). Still missing is a simple mechanistic theory that can make precise, quantitative predictions based on the mechanistic relationships between traits of the organisms in the different trophic levels and whole-ecosystem properties, such as carbon flux or recycling.…”