The acclimation hypothesis
The combination of the infra-red gas analyser and controlled environment rooms in the early 1960s led rapidly to the demonstration by experiment that photosynthetic capacity of leaves acclimates to the light environment in which individual plants are growing (e.g. Bjorkman & Holmgren 1963; Milner & Hiesey 1964; Gauhl 1976). Furthermore, it was shown that the degree of acclimation, and whether the efficiency of one or both of the carboxylation or photochemical processes was affected, depends on the ecotype, reflecting the environment to which the genotype had become adapted (Björkman 1981).
Subsequently, it was demonstrated both in situ and using excised branches that the photosynthetic capacities of leaves in canopies also acclimate to the light environment in which the leaves are growing. In spruce forest, for example, the photon-saturated rate of photosynthesis of leaves low in canopies was shown to be much less than that of leaves receiving much more irradiance higher up in the canopy (Jarvis, James & Landsberg 1976; Jarvis & Sandford 1986) and the shoots and leaves differed in a number of photosynthetic and structural properties, including leaf mass per unit area, leaf chlorophyll and RUBP carboxylase-oxygenase (Rubisco) activity (e.g. Lewandowska & Jarvis 1977). Indeed, there seemed to be some proportionality between the light received and the photosynthetic capacity at a level in a canopy, of a similar kind to that seen with plants grown in particular light environments in growth rooms (e.g. Leverenz & Jarvis 1980). Similar observations on canopies of other tree and herbaceous species led to several model-based studies to determine whether the composition of particular canopies was optimum with respect to the absorption of photons by leaves and their utilization in photosynthesis, taking into account features of canopy structure such as spatial distribution of leaf area density, leaf age and leaf inclination angles (e.g. Field 1983; Hirose et al. 1988).
Meanwhile, use of the photosynthesis model developed by Farquhar et al. (1980) to analyse response functions of photosynthesis of both plants grown in different light environments and leaves growing at different levels in canopies led to the conclusion that acclimation of photosynthetic capacity to irradiance was primarily through a shift in the parameter for maximum carboxylation, Vcmax (referred to henceforth as Va, µmol m−2 s−1), although close stochiometry between Va and the parameter for maximum electron transport, Jmax (referred to henceforth as Ja, µmol m−2 s−1) is usually found (Wullschleger 1993).
The last piece of evidence is the many observations made over the past 15 years of a linear relationship between photosynthetic capacity and leaf nitrogen concentration (e.g. Field & Mooney 1986; Chazdon & Field 1987; Anten, Schieving & Werger 1995; Reich et al. 1998). This relationship has proved to be robust, for example embracing a wide range of species grown with or without the addition of fertiliser and in ambient or elevated atmospheric CO2 concentrations (Medlyn et al. 1999; Peterson et al. 1999). The relationship arises because the enzyme responsible for carboxylation, Rubisco, may comprise over 30% of the protein in photosynthesizing leaves (Evans 1989; Lawlor 1993). However, these studies have tended to focus on variation among sun leaves from different species or sites, rather than on leaves within a single canopy. Although variations in leaf nitrogen concentration have been shown to correlate with changes in irradiance (Q) in that nitrogen and photosynthetic capacities are low in leaves growing at low Q (e.g. De Jong & Doyle 1985, Kull & Niinemets 1998; Carswell et al. 2000), there are fewer observations of gradients of leaf nitrogen concentration with respect to Q in tree canopies (e.g. Hollinger 1996; Dang et al. 1997; Bond et al. 1999). Nonetheless, the association between Q, Va and leaf nitrogen has been developed through studies in a number of canopies and it has been shown that a theoretically optimal distribution of nitrogen concentration maximizes canopy photosynthesis when the nitrogen concentration closely follows the distribution of Q, approaching zero when Q does (Field 1983; Chen et al. 1993, Kull & Jarvis 1995; Kruijt et al. 1997).
This association between Q, Va and leaf nitrogen has been perceived by ecosystem modellers as a parameter-efficient way to model canopy photosynthesis in soil-vegetation-atmosphere transfer (SVAT) models intended for incorporation into General Circulation Models (e.g. Sellers et al. 1992). In principle, provided that acclimation to Q is complete, if the photon-saturated rate of photosynthesis, or the leaf nitrogen concentration, is known at one level in the canopy, conventionally at the top, the rate of photosynthesis can readily be found at any level, given an appropriate light transmission model, and thus integrated canopy photosynthesis may be derived (e.g. Thornley & Johnson 1990; Sellers et al. 1992; Kull & Jarvis 1995; Kruijt et al. 1997; De Pury & Farquhar 1997). This idea has also been used to show that in such an ‘optimised’ canopy, photosynthesis may be predicted from Q absorption alone, as can leaf area index, given nitrogen availability (Haxeltine & Prentice 1996; Dewar 1996). It has become known as the acclimation hypothesis.
The initial objective of the investigation presented here was to test the assumption that acclimation could be regarded as complete, or ‘perfect’, in several different forest canopies, because there were indications that in some canopies this may be far from the case (e.g. Hollinger 1996; Kull & Niinemets 1998). The acclimation hypothesis requires that Va, determined by leaf nitrogen concentration, linearly covaries with the Q absorbed by a leaf, such that Va for any leaf in the canopy declines relative to the canopy-top value of Va in direct proportion to the Q absorbed by that leaf, also expressed as relative to the canopy-top value of absorbed Q. For complete acclimation, the relationship between relative Va and relative Q is therefore expected to be 1 : 1, and, crucially, to pass through the origin. If the relationship is other than this, additional parameters are required to calculate integrated canopy photosynthetic capacity, or site-specific descriptions must be employed (e.g. Sinoquet et al. 2001).
In this study, data sets from five forest canopies are analysed to test these predictions, and to assess to what extent photosynthetic capacity is uniquely related to Q or to other key variables such as leaf mass per unit area, across widely differing species, sites and vertical positions within each canopy. The five forest canopies comprise four broadleaf and one conifer stand from three geographically separate regions (central Scotland, southern England and the Amazon basin, Brazil). Relationships among vertical profiles in leaf Va, leaf nitrogen concentration and leaf mass per unit area are considered, together with the relationships between these parameters and Q within the canopies. The linearity of the in-canopy decline in both relative and absolute values of Va with Q is then tested, and the extent to which this decline can be predicted in different stands from simpler measurements of leaves at the bottom of the canopy is examined.