Water availability is widely recognized as a primary constraint on productivity of forest ecosystems (Breshears et al. 2005; Bréda et al. 2006). Drought has been implicated as the cause of large-scale decline in temperate forests (Allen 2009; van Mantgem et al. 2009), and global climate change has been predicted to increase the intensity and frequency of drought in many regions (IPCC 2007), including the Pacific Northwest of the United States (Mote & Salathé 2009). The effect of water stress on plant photosynthesis has been studied extensively and stomatal constraints on photosynthesis have become perhaps the most widely recognized physiological driver for reduced productivity under conditions of drought. However, water availability influences a number of other processes involved in tree growth, including cell expansion, phloem transport, nutrient transport and metabolic function. Each of these processes is critically important for growth and each represents a potential physiological bottleneck for productivity if water availability is limited. In order to more accurately predict tree and forest productivity under current and future climate regimes, the mechanistic relationships between drought and growth must be more fully understood.
Understanding the relationships between carbon supply and demand is important when investigating constraints on tree growth. Plants rely on both current photosynthesis and stored reserves of non-structural carbohydrates (NSC) for growth and other physiological functions. However, the extent to which trees are able to draw upon stored NSC has been questioned (Chapin, Schulze & Mooney 1990; Millard, Sommerkorn & Grelet 2007). When photosynthesis produces more carbon than is used for processes such as growth, reproduction and defence, some carbon is stored in the form of NSC. The concentrations of NSC in a tree are therefore indicative of the balance between carbon that has been fixed and the carbon that has been utilized for growth and metabolism or exuded below ground. The recurrent processes of assimilation, growth, reproduction and sometimes defence, result in periodic changes in the availability of, and demand for, mobile carbon. As such, concentrations of NSC in plants often show seasonal fluctuations (Fischer & Höll 1992; Newell, Mulkey & Wright 2002). Stored NSC potentially decouples assimilation from the processes in plants that require carbon, thereby facilitating growth and function during stressful conditions and recovery following disturbance (Iwasa & Kubo 1997). The fluctuating nature of the availability and demand for mobile carbon suggests that increased levels of NSC concentrations, particularly at any single moment, do not necessarily reflect an abundance of carbon. For example, NSC concentrations may increase as part of a regular annual cycle of accumulating reserves that later become largely depleted during leaf flush. Isolated measurements of NSC can therefore lead to an incomplete understanding of the carbon status of a tree and of the temporal dynamics of mobile carbon in trees. When evaluating the extent to which a tree is carbon limited, or the relative carbon limitations in different groups of trees, it is important to evaluate storage of NSC repeatedly throughout the year, particularly before and after key phenological events.
In a given environment, water stress increases with tree height. In the absence of transpiration, the gravitational component of water potential (Ψ) leads to a xylem tension gradient of 0.01 MPa m−1 increase in height (Scholander et al. 1965); and frictional resistance during transpiration leads to an additional path-length dependent reduction in Ψ (Mencuccini & Grace 1996; Ryan et al. 2000). Thus, an increase in tree height is in some ways comparable with occupying drier portions of an aridity gradient. Age and size-related reductions in productivity in forest stands and individual trees following canopy closure is a well-documented phenomenon (Jarvis & Leverenz 1983; Ryan & Waring 1992; Ryan, Binkley & Fownes 1997). Much of the research investigating constraints on growth associated with increased tree age and height has focused on carbon availability. These studies have investigated mechanisms including an increased ratio of respiration to photosynthesis following canopy closure (Yoda et al. 1965), and constraints on photosynthetic carbon gain because of path length-related resistance to xylem water transport (Ryan & Yoder 1997). However, studies examining NSC in trees under varying conditions of water availability have provided evidence that drought-related reductions in growth are not likely to be caused by constraints on carbon availability (Körner 2006; Millard et al. 2007; Sala & Hoch 2009). This lack of direct evidence for carbon availability limiting growth under conditions of water stress suggests that there is a mechanism involved in growth limitation during water stress that is not directly related to carbon gain. Constraints on turgor-driven cell expansion represent a mechanism for reduced growth that is directly related to water stress but unrelated to carbon availability. Cell expansion is driven by turgor (Lockhart 1965), and turgor has also been implicated as a factor in the regulation of cell division (Kirkham, Gardner & Gerloff 1972). In the absence of osmotic adjustment, turgor in developing cells will decline proportionally with xylem water potential (Boyer 1982). In view of the relationships between tree height, xylem water potential, turgor and processes involved in cell expansion and division, it has been hypothesized that height-related trends in stem elongation and foliar morphological characteristics may occur largely because of the influence of vertical gradients in water potential on turgor (Marshall & Monserud 2003; Woodruff, Bond & Meinzer 2004; Meinzer, Bond & Karanian 2008; Woodruff, Meinzer & Lachenbruch 2008). According to this hypothesis, growth is limited by reduced cell expansion rather than carbon supply. Constraints on growth as a result of reduced turgor under moderate drought conditions are consistent with reports that the first and most sensitive response to water stress in plants is a reduction in turgor-driven expansion of cells (Hsiao 1973; Hsiao et al. 1976; Bradford & Hsiao 1982; Larcher 1995).
For this study, we examined growth, water potential and tissue water relations of shoots, plus concentrations of NSC in foliage, small branches and trunk tissues at the tops and other portions of Douglas-fir trees of different heights. This work was done in order to investigate interrelationships between growth, water relations and storage of non-structural carbohydrates along a gradient of tree height. We sampled multiple times throughout a 17-month period in order to examine temporal variations in carbon balance. Tracking NSC in trees of different ages and sizes can provide information about the growth constraints of trees at different stages in their ontogeny. As explained previously, height influences tissue water relations in such a way as to function as a surrogate for an aridity gradient. As such, assessing NSC along a height gradient provides insight into how changes in climate conditions may influence source–sink relationships and overall growth in trees. Because phenology is largely driven by environmental cues that may change dramatically with predicted changes in climate because of increasing levels of atmospheric carbon dioxide, the phenological component of this study was included to provide additional insight into the potential impacts of climate change on forest productivity.