Photosynthesis and biomass both influence plant respiration—a new study by Alessio Collalti, Colin Prentice et al.

One of the greatest challenges in quantifying the global carbon balance is to correctly estimate how much carbon is accumulated in biomass versus how much is returned to the atmosphere as product of plant respiration. Alessio, Colin and others tackle this challenge in the recent paper published in Global Change Biology (Collalti et al., 2019). More specifically, the authors ask whether whole-plant respiration—the total amount of carbon converted from sugars to CO2 during cell respiration—depends exclusively on the amount of carbon produced during current photosynthesis or exclusively on the amount of respiring biomass. They found that neither was the case: whole-plant respiration depended on both photosynthesis and biomass, and also on carbohydrate storage. This finding has direct implications for correct determination of carbon balance of forests and how carbon partitioning is represented in global terrestrial vegetation models.

Plant respiration (R, g C m-2 yr-1) is the difference between gross primary productivity (P, amount of carbon fixed through photosynthesis) and net primary productivity (Pn, is the remaining carbon once respiratory costs are taken into account). Two main alternative hypotheses have been proposed which describe relationships between these three components:

  • Fixed ratio hypothesis suggests that Pn and P should be directly proportional to each other because R ultimately depends on the amount of photosynthates produced during photosynthesis (Waring et al., 1998). The idea that Pn:P is constant throughout the ontogeny and stand development would only be true if turnover rate was 100%. That is, the amount of new tissue and its respiratory demand equals that of dead tissue, which was just replaced.
  • The scaling hypothesis, following from the metabolic scaling theory, suggests that R should rather depend on biomass because biomass respires, so doubling biomass should result in doubling R (biomass and R scale isometrically with each other; Reich et al., 2006 and others). This hypothesis would necessarily imply that turnover rate is minimal. In other words, new respiring tissues are produced, but no tissues die.

To disentangle the photosynthesis vs. biomass dilemma, Collalti et al. (2019) simulated R, Pn and Pn:P patterns throughout a forest stand development. The simulations followed a process-based, ecophysiological model, which have been tested against long-term detailed observations of European beech stand in Sorø, Denmark.

Models and available literature have shown that a complete turnover of stem living cells within a single year is not possible—some stem cells live longer than that. This implies that whole-tree respiration cannot solely depend on carbon produced during current year photosynthates rejecting the fixed ratio hypothesis. In other words, respiration will depend not only on current-year photosynthates but also on the amount of previous-years respiring tissues as well as the amount of stored carbon in a form of non-structural carbohydrates.

On the other side, minimal turnover rates would lead to accumulation of far too large amount of new biomass, consequently leading to a huge respiratory carbon requirement, as indicated by the simulations (Fig. 1). Long-term, this strategy would not be sustainable and would lead to plant death. These results contradict the scaling hypothesis. When turnover rates were between 30% and 50% per year, simulations indicated that growth was limited because new photosynthates were diverted to replenishing NSC pools rather than to growth. But this was not the case for turnover rates >50%, which allowed for both growth and NSC refilling to occur simultaneously.

fig 2_collalti et al 2019
Figure 1. “Model results for (a) Pn:P ratio (dimensionless), (b) net primary production (Pn, g C m–2 yr–1) and, (c) autotrophic respiration (R, g C m–2 yr–1) performed with varying τ (turnover rate, coloured lines). The beginning of simulations correspond to 1950 (stand age 30 years); the end of simulations correspond to 2100 (stand age 180 years). The dark-pointed red line can be considered as a mechanistic representation of W98’s fixed P:P ratio (τ = 1 yr–1) while the dark pink line approximates R06’s scaling relationship between R and biomass (τ = 0.1 yr–1). Orange dotted lines represent Amthor’s (2000) (A00) ‘allowable’ range for the Pn:P ratio (0.65 to 0.2). The red dots give the average measured values (Wu et al. 2013) at the site for (a) Pn:P ratio, (b) Pn and (c) R. Vertical bars represent the standard deviation with horizontal bars representing the period 2006–2010 (stand age ~ 85–90 years). The shaded area represents the overall uncertainty of model results.” From (Collalti et al., 2019).

In conclusion, none of the two common hypotheses linking respiration, biomass and photosynthesis was supported. Rather the truth is somewhere in the middle, with both processes influencing respiration. But such a spectrum is broad and need further examinations to accurately project forest carbon balance in the future. Moreover, turnover rates and NSC reserves usage need to be taken into account in order to model carbon stocks and fluxes more accurately. This study also highlights the need for more observational studies and data on the dynamics of stem living cells and NSC supply and demand throughout the time.

 

Dr Collalti is a researcher from the both the National Research Council of Italy, Institute for Mediterranean Agriculture and Forest Systems (CNR-ISAFOM) and the Foundation Euro-Mediterranean Centre of Climate Change – Impacts on Agriculture, Forests and Ecosystem Services Division (CMCC-IAFES) in Italy. For more information about this paper, you can email Dr Collalti on alessio.collalti(at)isafom.cnr.it

 

Amthor, J. S. 2000. The McCree–de Wit–Penning de Vries–Thornley Respiration Paradigms: 30 Years Later. Annals of Botany 86: 1–20.

Collalti, A., M. G. Tjoelker, G. Hoch, A. Mäkelä, G. Guidolotti, M. Heskel, G. Petit, et al. 2019. Plant respiration: Controlled by photosynthesis or biomass? Global Change Biology.

Reich, P. B., M. G. Tjoelker, J.-L. Machado, and J. Oleksyn. 2006. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439: 457–461.

Waring, R. H., J. J. Landsberg, and M. Williams. 1998. Net primary production of forests: a constant fraction of gross primary production? Tree Physiology 18: 129–134.

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