When incident light levels drop below c. 20% of full sun, light availability becomes the most limiting resource for photosynthesis (Chazdon, 1988). Light limitation is particularly relevant in understory environments (Pearcy, 1990), shallow rivers partly shaded by riparian vegetation (Davies-Colley & Quinn, 1998) and sites with frequent occurrence of intermittent clouds (Knapp & Smith, 1988). These environments are characterized by sunflecks, defined as periods of relatively high light irradiance followed by periods of background low diffuse light. Although each sunfleck may last only seconds to minutes, sunflecks can contribute up to 80% of the total solar energy flux to the understory (Chazdon, 1988), thus being primary drivers for photosynthesis in these environments (Pearcy, 1990).
Stomatal movement mechanisms are key to the quantification of photosynthetic responses to variable light (e.g. Kirschbaum et al., 1988; Pfitsch & Pearcy, 1989; Ooba & Takahashi, 2003). The transport of osmoticum associated with stomatal opening is an active, energy-requiring mechanism (Zeiger, 1983; Assmann et al., 1985; Hanstein & Felle, 2002), and thus bioenergetic considerations are necessary to assess the ‘optimality’ of stomatal response times to sunflecks. A large number of experiments on leaf-level responses to step changes in light irradiance have been conducted over the past 30 yr with the aim of exploring stomatal delays in response to light changes. These experiments have shown large variations in stomatal delays (here denoted by the characteristic time scales of opening and closing, τop and τcl) across species and environmental conditions (Chazdon, 1988; Pearcy, 1990; Ooba & Takahashi, 2003). Despite such variability, there is general agreement that, when considering fully induced leaves, delays in stomatal response to variable light are the most relevant driver for leaf gas exchange, with biochemical delays occurring at much shorter time scales (Weber et al., 1985; Knapp & Smith, 1987, 1988). Furthermore, in most species, delays in stomatal opening appear to be shorter than delays in closing, that is τop < τcl (Ooba & Takahashi, 2003). Finally, the time scales associated with stomatal movements have been shown to be commensurate with sunfleck durations (Cardon et al., 1994; Naumburg et al., 2001), and to depend on the time of day and history of sunfleck occurrence (Kaiser & Kappen, 1997). The range of scales and environmental drivers involved complicate the quantification of the dynamic response of photosynthesis to light availability. Partly because of these complexities, the evolutionary causes of the variation in τop and τcl across species and growth conditions have not been fully addressed, despite the fact that delays in stomatal opening and closing have well-documented implications in terms of cumulative CO2 assimilation and transpiration (Naumburg et al., 2001) and, hence, leaf water use efficiency (WUE) (Knapp & Smith, 1989).
Ideally, perfectly tracking stomata (τop = τcl = 0 in Fig. 1) can fully exploit the available light during sunflecks, whilst minimizing the transpiration losses not associated with carbon gain by immediately closing the stomata when light decreases. However, delays between the change in light conditions and stomatal movement are inevitable because of inherent physical and biochemical limitations. When exploring various combinations of τop and τcl (Fig. 1), two other ‘end-member’ cases are worth considering: (1) fast opening stomata (τop ≅ 0) with a significant lag in closing (high τcl; points along the abscissa in the delay space of Fig. 1); and (2) fast closing stomata with a significant lag in opening (high τop and τcl ≅ 0, i.e. points on the ordinate in Fig. 1). In (1), the fast opening of stomata guarantees the ideal exploitation of available light during sunflecks, thus maximizing leaf cumulative photosynthesis (unless leaf water status worsens during the sunfleck; for example, Seastedt & Knapp, 1993). However, during the ensuing low light period, higher τcl causes more significant water losses through transpiration at times when assimilation is light limited. Conversely, in (2), the fast closure of stomata when light is abruptly reduced (τcl ≅ 0) minimizes the amount of ‘wasted’ water for transpiration, and the significant lags in stomatal opening when light is restored further contribute to the minimization of the water losses. These water savings have a negative effect on leaf carbon gain, because the delay in stomatal opening reduces assimilation. Hence, the delays in stomatal response affect WUE by altering both assimilation and transpiration. This conceptual exploration suggests the hypothesis that the most feasible combinations of stomatal delays in opening and closure represent a compromise between the need to maximize carbon gain and the need to minimize unproductive water losses (and, hence, the duration of periods under water stress), whilst simultaneously limiting energetic costs for stomatal movements. The case of perfect coordination between stomatal opening and closing (i.e. the 1 : 1 line in Fig. 1) does not necessarily represent the best solution. Rather, the optimal combination of delays will depend on a number of factors, including the plant ‘perceived values’ of water loss vs carbon gain, the average duration of the periods of light and darkness, and the energetic costs of moving stomata. The exploration of this delay space frames the objectives of this study.
Specifically, two inter-related questions pertinent to stomatal delays are addressed. We first investigate whether the measured delays in stomatal response and the asymmetry in opening/closing times noted in the literature can be broadly related to plant functional types and traits, such as drought and shade tolerance (which are expected to be associated with better light tracking stomata). Second, we assess whether the patterns in the observed delays can be explained by net carbon gain optimization, and how different values of τop and τcl may affect photosynthetic gains, transpiration losses and, more generally, the economics of leaf gas exchange. To address the first question, an extensive meta-analysis is conducted on stomatal responses to abrupt changes in light irradiance using published datasets. The second question is addressed by developing a dynamic model of leaf stomatal conductance and photosynthesis, coupled to a novel minimalist description of stomatal movement costs. This modeling approach provides a framework for exploring stomatal delays in the context of strategies adopted by plants to cope with light intermittency. We assess the dependence of these strategies on plant features, such as marginal WUE, stomatal movement cost parameters and ‘scaling laws’ relating stomatal conductance to aperture size.