Effects of Stomatal Delays on the Economics of Leaf Gas Exchange Under Intermittent Light Regimes

New Research Phytologist Effects of stomatal delays on the economics of leaf gas exchange under intermittent light regimes Giulia Vico1,2, Stefano Manzoni1,2, Sari Palmroth2 and Gabriel Katul1,2 1Civil and Environmental Engineering Department, Duke University, Box 90287, Durham, NC 27708-0287, USA; 2Nicholas School of the Environment, Duke University, Box 90328, Durham, NC 27708-0328, USA Summary Author for correspondence: • Understory plants are subjected to highly intermittent light availability and their Giulia Vico leaf gas exchanges are mediated by delayed responses of stomata and leaf bio- Tel: +1 919 660 5467 chemistry to light fluctuations. In this article, the patterns in stomatal delays across Email: [email protected] biomes and plant functional types were studied and their effects on leaf carbon Received: 13 April 2011 gains and water losses were quantified. Accepted: 5 July 2011 • A database of more than 60 published datasets on stomatal responses to light fluctuations was assembled. To interpret these experimental observations, a leaf New Phytologist (2011) 192: 640–652 gas exchange model was developed and coupled to a novel formulation of stoma- doi: 10.1111/j.1469-8137.2011.03847.x tal movement energetics. The model was used to test whether stomatal delays optimize light capture for photosynthesis, whilst limiting transpiration and carbon costs for stomatal movement. Key words: intermittent light, leaf economics, photosynthesis, stomatal • The data analysis showed that stomatal opening and closing delays occurred conductance, sunfleck. over a limited range of values and were strongly correlated. Plant functional type and climate were the most important drivers of stomatal delays, with faster responses in graminoids and species from dry climates. • Although perfectly tracking stomata would maximize photosynthesis and minimize transpiration at the expense of large opening costs, the observed combinations of opening and closure times appeared to be consistent with a near- optimal balance of carbon gain, water loss and movement costs. (e.g. Kirschbaum et al., 1988; Pfitsch & Pearcy, 1989; Introduction Ooba & Takahashi, 2003). The transport of osmoticum When incident light levels drop below c. 20% of full sun, associated with stomatal opening is an active, energy- light availability becomes the most limiting resource for requiring mechanism (Zeiger, 1983; Assmann et al., 1985; photosynthesis (Chazdon, 1988). Light limitation is partic- Hanstein & Felle, 2002), and thus bioenergetic consider- ularly relevant in understory environments (Pearcy, 1990), ations are necessary to assess the ‘optimality’ of stomatal shallow rivers partly shaded by riparian vegetation (Davies- response times to sunflecks. A large number of experiments Colley & Quinn, 1998) and sites with frequent occurrence on leaf-level responses to step changes in light irradiance of intermittent clouds (Knapp & Smith, 1988). These envi- have been conducted over the past 30 yr with the aim of ronments are characterized by sunflecks, defined as periods exploring stomatal delays in response to light changes. of relatively high light irradiance followed by periods of These experiments have shown large variations in stomatal background low diffuse light. Although each sunfleck may delays (here denoted by the characteristic time scales of last only seconds to minutes, sunflecks can contribute up to opening and closing, sop and scl) across species and environ- 80% of the total solar energy flux to the understory mental conditions (Chazdon, 1988; Pearcy, 1990; Ooba & (Chazdon, 1988), thus being primary drivers for photo- Takahashi, 2003). Despite such variability, there is general synthesis in these environments (Pearcy, 1990). agreement that, when considering fully induced leaves, Stomatal movement mechanisms are key to the quantifi- delays in stomatal response to variable light are the most cation of photosynthetic responses to variable light relevant driver for leaf gas exchange, with biochemical 640 New Phytologist (2011) 192: 640–652 Ó 2011 The Authors www.newphytologist.com New Phytologist Ó 2011 New Phytologist Trust New Phytologist Research 641 delays occurring at much shorter time scales (Weber et al., ideal exploitation of available light during sunflecks, thus 1985; Knapp & Smith, 1987, 1988). Furthermore, in most maximizing leaf cumulative photosynthesis (unless leaf species, delays in stomatal opening appear to be shorter water status worsens during the sunfleck; for example, than delays in closing, that is sop < scl (Ooba & Takahashi, Seastedt & Knapp, 1993). However, during the ensuing 2003). Finally, the time scales associated with stomatal low light period, higher scl causes more significant water movements have been shown to be commensurate with losses through transpiration at times when assimilation is sunfleck durations (Cardon et al., 1994; Naumburg et al., light limited. Conversely, in (2), the fast closure of stomata 2001), and to depend on the time of day and history of sun- when light is abruptly reduced (scl @ 0) minimizes the fleck occurrence (Kaiser & Kappen, 1997). The range of amount of ‘wasted’ water for transpiration, and the signifi- scales and environmental drivers involved complicate the cant lags in stomatal opening when light is restored further quantification of the dynamic response of photosynthesis to contribute to the minimization of the water losses. These light availability. Partly because of these complexities, the water savings have a negative effect on leaf carbon gain, evolutionary causes of the variation in sop and scl across spe- because the delay in stomatal opening reduces assimilation. cies and growth conditions have not been fully addressed, Hence, the delays in stomatal response affect WUE by alter- despite the fact that delays in stomatal opening and closing ing both assimilation and transpiration. This conceptual have well-documented implications in terms of cumulative exploration suggests the hypothesis that the most feasible CO2 assimilation and transpiration (Naumburg et al., combinations of stomatal delays in opening and closure rep- 2001) and, hence, leaf water use efficiency (WUE) (Knapp resent a compromise between the need to maximize carbon & Smith, 1989). gain and the need to minimize unproductive water losses Ideally, perfectly tracking stomata (sop = scl =0 in (and, hence, the duration of periods under water stress), Fig. 1) can fully exploit the available light during sunflecks, whilst simultaneously limiting energetic costs for stomatal whilst minimizing the transpiration losses not associated movements. The case of perfect coordination between sto- with carbon gain by immediately closing the stomata when matal opening and closing (i.e. the 1 : 1 line in Fig. 1) does light decreases. However, delays between the change in light not necessarily represent the best solution. Rather, the opti- conditions and stomatal movement are inevitable because mal combination of delays will depend on a number of of inherent physical and biochemical limitations. When factors, including the plant ‘perceived values’ of water loss exploring various combinations of sop and scl (Fig. 1), two vs carbon gain, the average duration of the periods of light other ‘end-member’ cases are worth considering: (1) fast and darkness, and the energetic costs of moving stomata. opening stomata (sop @ 0) with a significant lag in closing The exploration of this delay space frames the objectives of (high scl; points along the abscissa in the delay space of this study. Fig. 1); and (2) fast closing stomata with a significant lag in Specifically, two inter-related questions pertinent to sto- opening (high sop and scl @ 0, i.e. points on the ordinate in matal delays are addressed. We first investigate whether the Fig. 1). In (1), the fast opening of stomata guarantees 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 sop and scl 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 frame- work for exploring stomatal delays in the context of Fig. 1 Qualitative depiction of the role of the characteristic times of strategies adopted by plants to cope with light intermit- stomatal opening s and closing s on leaf gas exchange. The op cl tency. We assess the dependence of these strategies on plant experimentally observed combinations of sop and scl are hypothesized to be the result of evolutionary pressures to balance features, such as marginal WUE, stomatal movement cost carbon gains through photosynthesis, water losses through parameters and ‘scaling laws’ relating stomatal conductance transpiration and to reduce periods of water stress. to aperture size. Ó 2011 The Authors New Phytologist (2011) 192: 640–652 New Phytologist Ó 2011 New Phytologist Trust www.newphytologist.com

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