Abstract
Mechanistic photosynthesis models are at the heart of terrestrial biosphere models (TBMs) simulating the daily, monthly, annual and decadal rhythms of carbon assimilation (A). These models are founded on robust mathematical hypotheses that describe how A responds to changes in light and atmospheric CO2 concentration. Two predominant photosynthesis models are in common usage: Farquhar (FvCB) and Collatz (CBGB). However, a detailed quantitative comparison of these two models has never been undertaken. In this study, we unify the FvCB and CBGB models to a common parameter set and use novel multi‐hypothesis methods (that account for both hypothesis and parameter variability) for process‐level sensitivity analysis. These models represent three key biological processes: carboxylation, electron transport, triose phosphate use (TPU) and an additional model process: limiting‐rate selection. Each of the four processes comprises 1–3 alternative hypotheses giving 12 possible individual models with a total of 14 parameters. To broaden inference, TBM simulations were run and novel, high‐resolution photosynthesis measurements were made. We show that parameters associated with carboxylation are the most influential parameters but also reveal the surprising and marked dominance of the limiting‐rate selection process (accounting for 57% of the variation in A vs. 22% for carboxylation). The limiting‐rate selection assumption proposed by CBGB smooths the transition between limiting rates and always reduces A below the minimum of all potentially limiting rates, by up to 25%, effectively imposing a fourth limitation on A. Evaluation of the CBGB smoothing function in three TBMs demonstrated a reduction in global A by 4%–10%, equivalent to 50%–160% of current annual fossil fuel emissions. This analysis reveals a surprising and previously unquantified influence of a process that has been integral to many TBMs for decades, highlighting the value of multi‐hypothesis methods.
Highlights
As the gateway for carbon entry into terrestrial ecosystems, photosynthesis plays the keystone role in the biosphere of transferring atmospheric CO2 into terrestrial ecosystems
We ask the questions: (a) which processes are most influential for simulating carbon assimilation at various levels of atmospheric CO2 concentration and incident radiation, (b) which parameters are most influential, and (c) are the influential process and parameters different when considering absolute assimilation or the response of assimilation to a change in CO2? We further evaluate the outcome of this Sensitivity analysis (SA) using global terrestrial biosphere models (TBMs) simulations and measurements of leaf-scale photosynthesis
A novel, mathematically rigorous, process SA that accounts for both hypothesis and parameter variability in common models of photosynthesis has shown that limiting-rate selection was the most influential process, accounting for 57% of variation in A and 65% of variation in ΔA in response to a change in CO2
Summary
As the gateway for carbon entry into terrestrial ecosystems, photosynthesis plays the keystone role in the biosphere of transferring atmospheric CO2 into terrestrial ecosystems. Since its inception 40 years ago the Farquhar et al (1980; hereafter FvCB) model of C3 photosynthesis has revolutionized photosynthesis research (>5,000 citations, at time of writing). The FvCB model describes photosynthetic carbon assimilation (A) using a set of mathematically described hypotheses that represent the enzymatic subprocesses of photosynthesis and their integration, including: light-stimulated electron transport, CO2 fixation in the Calvin–Benson cycle and photorespiration. The FvCB model is an integrated set of mathematically described hypotheses, a system hypothesis, that yields quantitative predictions to accurately describe the dynamics of A in response to incident radiation (I), carbon dioxide concentration (Ca) and temperature. Observation, experiment and model-based photosynthesis research has seen substantive advances due to the availability of this mathematically rigorous hypothesis. Differing hypotheses for three key subprocesses distinguish the models: (a) electron transport, (b) limiting process selection, and (c) triose phosphate use (TPU)
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