A re‐evaluation of carbon storage in trees lends greater support for carbon limitation to growth

Abstract

We still have a poor understanding of what limits tree growth under many conditions. In general, tree growth can be limited by the availability of carbon within the plant (carbon limitation) or by the tree's ability to use the available carbon it has because of nutrient shortage, environmental conditions, or developmental constraints (sink limitation). A growing body of literature suggests that current tree growth is sink limited under most conditions, with much of the evidence inferred from trees' high levels of nonstructural carbon (NSC). These inferences rely on the assumption that carbon storage is passive and that NSC does not accumulate when growth is carbon limited (Bansal & Germino, 2008). However, storage may be an active process, occurring at the expense of growth (Chapin et al., 1990; Lacointe et al., 2004; Genet et al., 2010). We argue that carbon starvation – even if it does not occur every year or even every decade in the life of a tree – is crucial to understanding carbon storage and carbon limitation in trees. We define carbon starvation, modified after McDowell (2011), as the outcome of insufficient carbon supply from current photosynthesis and available storage to sustain the metabolism, regeneration, or defense necessary for immediate survival (Fig. 1). Episodes of carbon starvation (past and present) may have led to the evolution of conservative allocation strategies favoring greater reserve formation at the expense of potential growth. Therefore, an increase in carbon storage and decrease in growth could be a plastic or evolutionary response to carbon-limiting conditions – not a result of sink limitation. To illustrate this point, we reexamine two phenomena relevant to the active debates regarding carbon limitation: tree growth at alpine treeline and under water stress. Scheme for carbon supply and allocation to three groups of plant functions. The order of groups indicates carbon allocation priorities, with competition for carbon occurring among processes in the same group. The order within a group does not indicate priority, however it is assumed that some priority structure does exist and can change. Group I includes carbon needs essential to immediate survival. Carbon starvation occurs when the amount of available carbon is less than that required by Group I processes. Group II includes processes which are not immediately necessary for survival, but may affect survival or fitness in the long run. For a given tree, the allocation hierarchy is determined by its life-history strategy as well as inter- and intra-annual plasticity in response to environmental cues or carbon status. Growth (or any process) can become more carbon limited by (1) a decrease in available carbon, (2) an increase in Group I requirements, or (3) increased allocation to other processes (such as active storage) within Group II. Even though active storage can contribute to the available carbon pool, it may only do so selectively for particular uses. Finally, if Group II processes become carbon saturated (sink limited), only then will carbon be allocated to Group III, which includes overflow functions, such as passive storage. We believe that passive storage is rare, and argue that most nonstructural carbon is actively stored, which can occur when growth is still carbon limited. Carbon storage, defined here as formation of nonstructural carbon compounds that 'can be mobilized in the future to support biosynthesis', can be either passive or active (Chapin et al., 1990). Passive storage forms an excess pool when carbon supply is greater than carbon demand of other processes, such as growth (Fig. 1). Active storage, or reserve formation, on the other hand, occurs when carbon is directed into storage at the expense of growth or other processes. Reserve formation allows a tree to prepare for (1) predictable asynchrony of supply and demand for carbon (e.g. early spring growth for deciduous trees) and (2) unpredictable emergencies such as disturbances that affect carbon gain or need (Chapin et al., 1990). The potential for active reserves is often ignored when inferring the nature of growth limitation. When comparing trees in different sites or treatments, sink limitation is incorrectly inferred from one of two main patterns: (1) higher NSC content together with lower growth rates (Hoch & Körner, 2003; Würth et al., 2005; Palacio et al., 2008; Sala & Hoch, 2009), or (2) relatively stable NSC levels throughout the year that do not decline to zero (Hoch et al., 2002, 2003; Shi et al., 2008). The rationale for inferring sink limitation from the first pattern is that NSC pool size is the difference between carbon gain (source) and carbon demand (sink) within the plant (Körner, 2003). This assumption is true if all storage is passive, but not if it is active (Lacointe et al., 2004; Bansal & Germino, 2008; Genet et al., 2010). Reduced growth and increased storage is also consistent with carbon limitation if (a) populations vary