On the Relationship between Shade Tolerance and Shade Avoidance Strategies in Woodland Plants

Abstract

Decreasing light availability with time is one of the primary factors that drives autogenic succession in woodland communities. In many successions, the pattern of species replacement appears to be largely a consequence of a negative correlation across species between adaptation to high irradiance and adaptation to low irradiance (Bazzaz 1979, Oliver and Larson 1990, Kobe et al. 1995). The mechanistic basis for this negative correlation can be explained with respect to at least two distinct fitness components: 1) the maximization of light interception and 2) the maximization of net carbon fixation per unit leaf protein (Givnish 1988). A plant grown under high irradiance can maximize light interception through a highly branched, bushy growth form (Steingraeber et al. 1979, Shukla and Ramakrishnan 1986). Maximum net carbon fixation under high irradiance is achieved through sun-adapted leaf physiology (Bj6rkman 1981). In contrast, for a plant grown under low irradiance, light interception is maximized through strong vertical growth (King 1990), and net carbon fixation is maximized through shadeadapted leaf physiology (Bjdrkman 1981). The term has long been used to describe the suite of leaf-level traits that afford maximal net carbon fixation under low irradiance. Less commonly, the analogous term has been used to describe the suite of architectural traits that contribute to strong vertical growth in plants grown under low irradiance (Grime 1966, Smith 1986, 1994). Although many components of shade tolerance and shade avoidance have been studied along light gradients, the relationship between these strategies has received very little theoretical and empirical attention (Kuppers 1994). Do they represent alternative adaptations to light limitation with patterns of covariance that reflect tradeoffs through life history or phylogenetic constraints (Smith 1986)? Alternatively, are the distributions across taxa, of shade avoidance and shade tolerance, independent of each other? In this paper, we briefly review the mechanistic basis of shade tolerance and shade avoidance to illustrate that both of these strategies can be expected to impose costs (trade-offs) to a plant in terms of reduced relative growth rate under high irradiance (Fig. 1). By interpreting these costs in the context of different selection regimes within vegetation, we arrive at the prediction that shade tolerance and shade avoidance strategies should be generally negatively correlated along light gradients.