Nighttime Stomatal Conductance and Transpiration in C3 and C4 Plants

Abstract

Histogram summarizing reported g night in species among different plant functional groups. For each species, g night was averaged from all reported values with units in mol m−2 s−1 presented in Supplemental Table S1 and thus represents a mixture of field and greenhouse studies. The black two-headed arrow at the top left of the graph represents the range for reported g cuticular taken from many species, and reported g night within this range may be largely due to g cuticular rather than g stomatal. A complete listing of species with references is provided in Supplemental Table S1. The magnitude of water loss occurring during the night depends on both g night and the vapor pressure difference (VPD) between leaves and the air, as well as canopy structure and atmospheric mixing. While g night has been recorded at up to 90% of daytime conductance, nighttime VPD is typically much lower than daytime. Thus, nighttime transpiration rates (E night) are typically 5% to 15% of daytime rates, although sometimes as high as 30%, based on gas exchange measurements of individual leaves, whole-plant sap flow, and field scale lysimetry (Benyon, 1999; Snyder et al., 2003; Bucci et al., 2004, 2005; Daley and Phillips, 2006; Scholz et al., 2007). While some methods are more accurate and/or have less uncertainty than others, a few studies have compared methods, generally finding agreement even across measurement scales (e.g. leaf versus whole plant; Green et al., 1989). Drawbacks for each method must be recognized, particularly when comparing species or environments. For example, leaf-level gas exchange typically includes cuticular as well as stomatal components of leaf conductance to water vapor, while sap flow methods typically have attendant uncertainties as to the proportion of the measured flux resulting in bole refilling rather than transpiration from the canopy. Nevertheless, there is broad agreement among the methods and scales that stomata of many species remain partially open during the night. Measurements of minimum leaf conductance induced by ABA application and by drying excised leaves to wilting have been used to separate stomatal (g stomatal) and cuticular (g cuticular) conductance (Rawson and Clarke, 1988; Howard and Donovan, 2007). Conductance measured at maximal stomatal closure can be functionally defined as g cuticular because it is not under guard cell regulation. For a few species, this would include the effect of dust or stomatal plugs that prevent complete closure (Feild et al., 1998). In general, g cuticular estimates range from 0.004 to 0.020 mol m−2 s−1 (Rawson and Clarke, 1988; Nobel, 1991; Kerstiens, 1995; Boyer et al., 1997; Burghardt and Riederer, 2003; Howard and Donovan, 2007), far lower than most estimates of g night (Fig. 1; Supplemental Table S1). Thus, most reported values of g night are largely influenced by g stomatal. Diagram summarizing sources of variation (internal and external) affecting g night and transpiration (E night), and consequences of g night and E night at the individual plant and larger scales. Species in which g night has been documented include a diverse range of genera and life forms (annuals and perennials; monocots, herbaceous dicots, shrubs, and trees; Fig. 1; Supplemental Table S1) native to a diversity of habitats: e.g. wetland (Loftfield, 1921), desert (Donovan et al., 2003; Snyder et al., 2003; Ludwig et al., 2006), neotropical savanna (Bucci et al., 2004, 2005; Domec et al., 2006; Scholz et al., 2007), temperate deciduous and evergreen forests (Benyon, 1999; Oren et al., 2001; Barbour et al., 2005; Daley and Phillips, 2006; Kavanagh et al., 2007), and subalpine forest (Herzog et al., 1998). Many horticultural and crop species have substantial g night and/or E night (England, 1963; Rosenberg, 1969; Rawson and Clarke, 1988; Green et al., 1989; Blom-Zandstra et al., 1995; Assaf and Zieslin, 1996; Musselman and Minnick, 2000). Although it has been suggested that sustained nocturnal stomatal opening is not a feature of grasses (Loftfield, 1921), substantial g night has been observed in Distichlis spicata (C4; Snyder et al., 2003) and wheat (Triticum aestivum; C3; Rawson and Clarke, 1988), among others. Substantial variation in magnitude of maximum g night has been observed among closely related species (Supplemental Table S1); however, differences among some species are minimal and not biologically significant (see Helianthus species, Supplemental Table S1; Howard and Donovan, 2007). Multiple surveys have shown that g night varies substantially among species within a particular environment or habitat type (Snyder et al., 2003; Bucci et al., 2004; Daley and Phillips, 2006; Kavanagh et al., 2007), and the relationship of species differences to source environment or habitat remains unclear. Additional studies investigating g night in a phylogenetic context in native and common garden locations will be required to determine whether species differences in g night are adaptiv