Moving beyond photosynthesis: from carbon source to sink‐driven vegetation modeling

Abstract

Knowledge of future terrestrial carbon (C) pools and fluxes is based on simulations by Dynamic Global Vegetation Models (DGVMs; Cox et al., 2000; Sitch et al., 2008). For simplicity we used the DGVMs acronym to include all of the models able to simulate C and vegetation dynamics at large spatial scales, which are sometimes referred to as Terrestrial Biosphere Models, Terrestrial Ecosystem Models, vegetation components of Earth System Models, and Land Ecosystem Models. DGVMs are now typically coupled to climate models to account for biophysical and biogeochemical feedback caused by vegetation (Bonan, 2008; Chapin et al., 2008; Anderson et al., 2011). The ultimate aim is to simulate climate–vegetation dynamics that explicitly account for mutual interactions and thus provide us with a better spatiotemporal description of water fluxes together with the most realistic scenarios for the future climate and C cycle (Friedlingstein et al., 2006; Thornton et al., 2007; Bonan et al., 2011). Current DGVMs are simulating long-term tree and forest stand growth as a consequence of the amount of assimilated C, triggering an inevitable positive feedback between C assimilation and growth. The key factors affecting stomatal aperture and C assimilation are atmospheric CO2 concentration, water availability, light, vapor pressure deficit and temperature (Sellers et al., 1997; Lawson et al., 2011). However, direct control of C sinks (defined as growth in the sense of C investment on plant tissue expansion) via environmental factors has been shown to be more important than indirect control via photosynthesis (the C source, see Fig. 1). For example, water- or temperature-limited plants tend to reduce growth but increase C storage (Körner, 2003; Sala & Hoch, 2009; Woodruff & Meinzer, 2011; Sala et al., 2012), which suggests that environmental controls act first on sink activity rather than source activity (Körner, 2013). Nevertheless, in all existing DGVMs, plant growth is driven by photosynthesis directly without considering water and thermal limitations via metabolic, cambial and meristematic activity (blue arrows in Fig. 1; Bonan et al., 2003; Sitch et al., 2003; Krinner et al., 2005). The entire photosynthesized net C (the source) is then partitioned among different C pools, mostly based on allometric rules derived from observations (Poorter et al., 2012) or using simplified functional allocation schemes (Friedlingstein et al., 1998; Franklin et al., 2012). Allocation to carbohydrate reserves, root exudates and export to symbionts are mostly missing. This opens up a huge discrepancy between the way plant growth is modeled today (blue arrows in Fig. 1) and the way it is understood based on experimental evidence (red arrows in Fig. 1). In this article, we suggest a revised hierarchy of plant growth control by removing the causal link from C assimilation to plant growth and by providing a description of the mechanistic connections among processes. Available soil water, temperature, nutrients, light, and CO2 are indisputably the key drivers of plant growth (Boisvenue & Running, 2006; McMurtrie et al., 2008; Ågren et al., 2012; Fig. 1). The former three (water, temperature, and nutrients) are fundamentally different from the latter two (light and CO2) because they can affect both sink and source activities, while light and CO2 only affect the source activity (C assimilation, Fig. 1). In this section, we compare the hierarchy of such limitations based on experimental evidence, which will lead into the discussion of strategies for modeling plant growth. When water limitations occur, there is evidence that cambial and leaf growth are inhibited at much lower levels of water stress (higher water potentials) than photosynthesis (Fig. 2; Boyer, 1970; Hsiao, 1973; Hsiao et al., 1976; Muller et al., 2011; Tardieu et al., 2011). Because organ expansion is affected earlier and more intensively than photosynthesis, plants experiencing soil water deficit often accumulate nonstructural carbohydrates (NSC) and reduce growth (Würth et al., 2005; Woodruff & Meinzer, 2011). Drought stressed or more apical parts of trees show lower xylem- or leaf-water potential than well-watered or more basal parts. This decrease in xylem- or leaf-water potential implies a reduction in cell turgor and in the capacity to transport sugars (Woodruff et al., 2004; Sala et al., 2011; Woodruff & Meinzer, 2011). Specifically, lower cell turgor has the potential to limit cell wall expansion, cell wall synthesis and protein synthesis (Lockhart, 1965; Hsiao, 1973; Sala et al., 2011). This means that C assimilation continues while sink activity (tissue growth) is inhibited, which most likely explains the accumulation of NSC in stressed plants (Körner, 2003). For example, Sala & Hoch (2009) showed that in Pinus ponderosa, mobile C compounds increase with increasing tree height. The possibility of plants actively prioritizing storage over growth allows additional interpretations o