Notes On the Ecophysiology of Photosynthesis (last updated in 2000)

1. INTRODUCTION
Plant ecophysiological research has made significant advances in understanding canopy-atmosphere interactions during the last 30 years. For example, a series of biochemical models of leaf photosynthesis have been developed that describe CO2 assimilation in relation to environmental conditions as limited by enzyme kinetics, photochemistry, and carbon metabolism (Farquhar et al. 1980, Sharkey 1985, Collatz et al. 1991, 1992). In addition, much has been learned about the ecology of leaf traits and the various structural and growth strategies employed by plants from a diversity of biomes (e.g. Field and Mooney 1986, Reich et al. 1992).

Biochemical models have proven useful for elucidating the ecological consequences of leaf biochemistry on plant carbon gain (Cowan 1986, Farquhar 1989, Field 1991, Chen et al. 1993), while comparative analysis of leaf traits has revealed striking generalities about leaf structure and function and plant growth (Reich et al. 1997, Reich et al. 1999c). Despite the distinct perspectives of these two approaches, they are quite complementary in many regards and are, in fact, converging on similar hypotheses of the evolution and functional ecology of carbon gain.

2. ECOLOGY OF LEAF TRAITS



Figure 1.  Conceptual  model of the interrelationships among various plant traits. See text for details. From Reich et al. (1992).

Numerous studies have focused on the ecology of carbon gain from the standpoint of plant nutrition, growth habit, and leaf structure (e.g. Small 1972, Stoner et al. 1978, Chapin 1980, Chabot and Hicks 1982, Mooney and Gulmon 1982, Field and Mooney 1986, Kikuzawa 1991). Reich et al. (1992) summarized much of this work by focusing on leaf life-span as an “ecological integrator” that  universally relates leaf, plant, and ecosystem traits (Figure 1). Reich et al. (1991a, 1991b,1992), and subsequent studies (Ellsworth and Reich 1993, Reich 1993, Reich et al. 1994, Reich and Walters 1994, Reich et al. 1995, Reich et al.1997, Reich et al. 1998a, 1998b, 1998c, 1998d, 1998e), quantitatively demonstrate the generality of relationships between leaf life-span and net photosynthesis (Amax), specific leaf area (SLA), leaf nitrogen (N), leaf respiration (R), stomatal conductance (gmax), and whole plant relative growth rate (RGR). Collectively, these studies suggest that there are “fundamental global patterns of variation among leaf structure, longevity, metabolism, and chemistry” (Reich et al. 1997).

The underlying notion to the “Reich equations”  is that there must be some balance between a plant’s material investment in a leaf and the income gained from it (Orians and Solbrig 1977, Mooney and Gulmon 1979, Chabot and Hicks 1982). The interrelationships outlined in Figure 1 can be applied to “young, individual, open-grown plants, and to forest stands” (Reich 1992). For example, fast-growing plants generally have leaves with short leaf life-spans, high SLA and N. This, in turn, is consistent with high Amass and RGR, resulting in high plant carbon gain and growth that “feed back” to result in higher leaf area and mass, further accelerating carbon gain, growth rate, and leaf turnover rate (Reich et al. 1992). Conversely, slow-growing plants typically exhibit opposite traits (e.g. low SLA, Amass) that interact to result in low carbon gain and growth. However, as the plant matures, the extended leaf life-spans lead to an accumulated of high leaf mass and leaf area that act to partially compensate for low productivity traits (Reich et al. 1992).

Thus, the characteristics common to plants with short leaf life-spans may be summarized as “short leaf longevity syndromes” (Kikuzawa 1995). Such plants tend to live in resource rich soils and exhibit high RGR, with high Amax and low construction costs. On the other hand, plants in resource poor soils have “long leaf longevity syndromes” with low RGR, low Amax and high construction costs (Kikuzawa 1995). Further, these leaves are generally thicker (lower SLA) than those adapted to resource rich soils.

A strong positive correlation between SLA and Nmass (nitrogen content on a mass basis) is often observed across species from different habitats (e.g. Schulze et al. 1994, Reich et al. 1997) while the opposite trend is often found within canopies (e.g. Gutschick and Wiegel 1988, Reich et al. 1994). Growth conditions (light, temperature, moisture, and nutrient availability) apparently determine the minimum sunlit SLA across sites while vertical variations in SLA from the top to the bottom of a canopy are strongly influenced by light availability and the potential for photosynthesis (Gutschick and Wiegel 1988).

As noted by Schulze et al. (1994), the interspecific relationship between Nmass and SLA is not straightforward. Thin, high SLA, short life-span leaves with low Amax are unlikely to be found because low photosynthesis for a short duration gives only low productivity over the life-span of the leaf and does not provide adequate carbon gains to payback the costs of leaf construction and maintenance (Chabot and Hicks 1982, Williams et al. 1989, Kikuzawa 1991). This is clearly not advantageous. On the other hand, thick, long life-span leaves with high Amax are unlikely as well because light penetration in such a leaf would be so limited (Terashima and Hikosaka 1995) that much of the leaf resources (N) would go unused (Reich and Walters 1994). Furthermore, the chances of herbivory dramatically increase for a highly palatable leaf displayed for a long periods of time (Reich et al. 1992).

Further, Givnish (1979) argues that leaves are generally thicker in dry and nutrient-poor habitats than elsewhere. In these environments, nutrient availability and photosynthetic capacity are typically low while temperature and evaporative demand can be high. Water is too costly for transpirational cooling and water use efficiency is best maximized through morphological adaptations that minimize the evaporative demand at the leaf surface. Such xeromorphic adaptations include increased leaf thickness with low surface-area-to-volume ratios, well developed cuticular layers with abundant epicuticular waxes, thick-walled epidermis, stomata located in pits (e.g. conifer needles), and leaf pubescence (Stenberg et al. 1995), all which act to decrease SLA and Nmass.

Leaves from nutrient poor sites or with low N and Amax, tend to have longer leaf life-spans and tend to be highly protected from herbivory by high concentrations of leaf tanins and phenols (Mooney and Gulmon 1982) which should further act to decrease SLA and Nmass. Thus, for a multitude of ecological and biophysical reasons, interspecific variation in SLA correlates with Nmass. Indeed, the generality of this relationship is the basis for SLA modulating photosynthesis-nitrogen relationships (e.g. Reich et al. 1998a).



 
3. THE LEAF BIOCHEMISTRY MODEL


Figure 2. Coordination of light reactions and Calvin cycle via interdependence on ATP and NADPH in the chloroplast. From Campbell (1993).

In summarizing more than 10 years of research, Farquhar and von Caemmerer (1982) identified and mathematically represented several key aspects of leaf biochemistry (Figure 2), namely (1) production of ATP and NADPH, and their coordination with consumption, (2) a regeneration limitation on CO2 fixation, and (3) the modeling of electron transport as a function of absorbed light and potential transport, thereby introducing “photosynthetic control”, based either on the availability of ADP for phosphorylation or of NADP for reduction (Cheeseman and Matej Lexa 1996). Recent ecological-evolutionary theories of coordination between photochemistry and biochemistry (Cowan 1986, Chen et al. 1993) and thus between light absorption and photosynthetic capacity (Farquhar 1989, Field 1991), are natural extensions of the basic assumptions of Farquhar and von Caemmerer. In short, for theoretical and biochemical reasons, photosynthetic capacity (i.e. Amax) appears to be linearly related to the average absorbed irradiance, with the proportionality constant equal to the quantum yield of photosynthesis (φ), a fairly conservative parameter (Ehleringer and Bjorkman 1981).

4. CONVERGENCE OF BIOCHEMICAL AND ECOLOGICAL APPROACHES         
The biochemical and ecological approaches are converging on similar hypotheses of leaf ecophysiology. Both approaches are based on theories of resource optimization. Ecological analysis of the biochemistry of photosynthesis (Cowan 1986, Farquhar 1989, Field 1991, Chen et al. 1993), that is, application of functional convergence theories, suggests mechanisms, namely N allocation, by which leaves and canopies acclimate to light availability such that Amax correlates with mean absorbed irradiance. Plants are so efficient that they tend not to acquire what they cannot use. While overinvestment in light energy would appear to ensure a plentiful supply of light to drive carbon fixation, it will actually inhibit photosynthesis (i.e. photoinhibition) through damage to the photosynthetic apparatus (Osmond 1994).

In contrast, but complementary to the biochemical approach, studies by Reich et al. and others (e.g. Field, Schulze, Kikuzawa), provide empirical evidence suggestive of global convergence in plant functioning such that Amax correlates with N allocation to leaves. The Reich equations, however, are more related to the “costs of doing business” rather than the business itself (i.e. photosynthesis). Consistent with this perspective, leaf traits are generally expressed per unit leaf mass rather than per unit leaf area. Mass-based expressions simply reflect total plant investment better than one-dimensional area-based expressions.

Aside from their convergence and complementary aspects, the biochemical approach is more useful for ecosystem and global models than the Reich equations for two reasons. First, while both allow prediction of Amax, the Reich equations are empirical. As such, their application to species and ecosystems not used in their parameterization is problematic. Their validity relies on whether or not the particular plants used are representative of all global vegetation types. Second, although Reich et al. (1998a) contend that “the relationships...could be used...to predict Amax for given species, functional types, or community types with known or typical levels of SLA and/or N”, the latter are known no better than Amax at the global. The biochemical approach, or the simpler light-response version (Pmax = φImean), is based on the mechanisms of photosynthesis which are fundamentally the same among all photoautotrophs (Collatz et al. 1998). Further, it can be applied globally using standard meteorological data (I, Tair) and satellite observations (NDVI).

Finally, the convergence of the biochemical and ecological approaches would be even greater if the suite of leaf traits on which the Reich equations are based included leaf light absorption. Indeed, light absorption, because it reflects leaf investment in light energy capture and electron transport, should be a better indicator of Amax than leaf N, which is only indirectly related to Amax because a significant portion of leaf N (~50%) is contained in photosynthetic enzymes and proteins (Chapin et al.1987). Light absorption (the absolute value of light absorbed), as opposed to light absorptance (the fraction of light absorbed), is probably overlooked as a key leaf trait, in part, because it is difficult to measure. Furthermore, it is not portable like leaf N. There is a certain elegance in being able to diagnose, without any knowledge of the species or the environment form which it came, the photosynthetic potential of a leaf solely from its chemical composition.

Determination of leaf absorption requires measurement of absorption (not difficult) under natural light conditions at the leaf’s natural angle of inclination and compass orientation (difficult). Measurement of canopy light absorption is thus much easier (e.g. with above and below-canopy sensors). I know of no study in which both Amax and light absorption were measured for the same leaves under natural field conditions. Assuming canopy Amax can be derived from eddy covariance measurements of net ecosystem CO2max and light absorption, albeit at the canopy scale. exchange, networks such as AmeriFlux and EuroFlux could potentially provide a large dataset with which to examine the relationship between Amax and light absorption, albeit at the canopy scale.

5. CONCLUSION
Over the last 15 years, the work of Reich et al. has revealed that “despite striking differences in climate, soils, and evolutionary history among diverse biomes ranging from tropical and temperate forests to alpine tundra and desert”, similar interspecific relationships exist among leaf life-span and mass-based expressions of leaf photosynthetic capacity (Amax), specific leaf area (SLA), nitrogen content (N), and respiration (R).  Working from a generalized biochemical model of photosynthesis (Farquhar and von Caemmerer 1982) several authors have argued that the enzymatic capacity for photosynthesis should correlate with the potential for light-driven electron transport. Thus, Amax should correlate with light absorption (Amax=φImean).

Despite the distinct perspectives of these two approaches, they are quite complementary in many regards and are, in fact,  converging on similar hypotheses of the evolution and functional ecology of carbon gain. The “Reich equations”, however, because of their empiricism and dependence on chemical and structural leaf characteristics that are not easily defined at the global scale, are less applicable to global models than the “biochemical equations” which require readily available standard meteorological data (I, Tair) and satellite observations (NDVI).




REFERENCES

Chabot,BF; Hicks,DJ (1982): The ecology of leaf life spans. Annu. Rev. Ecol. Syst. 13, 229-259.

Chapin,FS (1980): The mineral nutrition of wild plants. Annu. Rev. Ecol. Syst. 11, 233-260.

Chapin,FS; Bloom,AJ; Field,CB; Waring,RH (1987): Plant responses to multiple environmental factors. BioScience 37, 49-57.

Cheeseman,JM; Lexa,M (1996): Gas exchange:Models and measurements. In: Photosynthesis and the environment. Vol. 5. (Ed: Baker,NR) Kluwer Academic Publishers, Dordrecht, 223-240.

Chen,JL; Reynolds,JF; Harley,PC; Tenhunen,JD (1993): Coordination theory of leaf nitrogen distribution in a canopy. Oecologia 93, 63-69.

Collatz,GJ; Ball,JT; Grivet,C; Berry,JA (1991): Physiological and environmental regulation of stomatal conductance, photosynthesis and transpiration: a model that includes a laminar boundary layer. Agricultural and Forest Meteorology 54, 107-136.

Collatz,GJ; Ribas-Carbo,M; Berry,JA (1992): Coupled photosynthesis-stomatal conductance model for leaves of C4 plants. Aust. J. Plant Physiol. 19, 519-538.

Cowan,IR (1986): Economics of carbon fixation in higher plants. In: On the economy of plant form and function. (Ed: Givnish) Cambridge University Press, Cambridge, 133-170.

Ehleringer,J; Bjorkman,O (1977): Quantum yields for CO2 uptake in C3 and C4 plants. Plant Physiol. 59, 86-90.

Ellsworth,DS; Reich,PB (1993): Canopy structure and vertical patterns of photosynthesis and related leaf traits in a deciduous forest. Oecologia 96, 169-178.

Farquhar,GD (1989): Models of integrated photosynthesis of cells and leaves. Philosophical Transactions of Royal Society of London B 323, 357-367.

Farquhar,GD; von Caemmerer,S (1982): Modeling of photosynthetic response to environmental conditions. In: Physiological Plant Ecology II. Vol. 12B. (Eds: Lange,OL; Nobel,PS; Osmond,CB; Ziegler,H) Springer-Verlag, Berlin, 549-587.

Farquhar,GD; von Caemmerer,S; Berry,JA (1980): A biochemical model of photosynthetic CO2 fixation in leaves of a C3 species. Planta 149, 78-90.

Field,CB (1991): Ecological scaling of carbon gain to stress and resource availability. In: Response of plants to multiple stresses. (Eds: Mooney,HA; Winner,WE; Pell,EJ) Academic Press, San Diego, 35-65.

Field,C; Mooney,HA (1986): The photosynthesis-nitrogen relationship in wild plants. In: On the economy of plant form and function. (Ed: Givnish,TJ) Cambridge University Press, Cambridge, 22-55.

Givnish,T (1979): On the adaptive significance of leaf form. In: Topics in Plant Population Biology. (Eds: Solbrig,OT; Jain,S; Johnson,GB; Raven,PH) Columbia University Press, New York, 375-407.

Gutschick,VP; Wiegel,FW (1988): Optimizing the canopy photosynthetic rate by patterns of investment in specific leaf mass. Amer. Natur. 132, 67-86.

Kikuzawa,K (1991): A cost-benefit analysis of leaf habit and leaf longevity of trees and their geographical pattern. Amer. Natur. 138, No 5, 1250-1263.

Kikuzawa,K (1995): The basis for variation in leaf longevity of plants. Vegetatio 121, 89-100.

Mooney,HA; Gulmon,SL (1982): Constraints on leaf structure and function in relation to herbivory. BioScience 32, 198-206.

Orians,GH; Solbrig,OT (1977): A cost-income model of leaves and roots with special reference to arid and semiarid areas. Amer. Natur. 111, 677-690.

Osmond,CB (1994): What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Photoinhibition of photosynthesis: From molecular mechanisms to the field. (Eds: Baker,NR; Bowyer,JR) Bios Scientific Publishers, Oxford,UK, 1-24.


 


Reich,PB (1993): Reconciling apparent discrepancies among studies relating life span, structure and function of leaves in contrasting plant life forms and climates: 'the blind men and the elephant retold'. Functional Ecology 7, 721-725.

Reich,PB; Ellsworth,DS; Walters,MB (1998a): Leaf structure (specific leaf area) modulates photosynthesis-nitrogen relations:evidence from within and across species and functional groups. Functional Ecology 12, 948-958.

Reich,PB; Ellsworth,DS; Walters,MB; Vose,J; Gresham,C; Volin,JC; Bowman,W (1998e): Generality of photosynthetic and associated leaf traits relationships: a test across six biomes. Ecology, .

Reich,PB; Kloeppel,BD; Ellsworth,DS; Walters,MB (1995): Different photosynthesis-nitrogen relations in deciduous hardwood and evergreen coniferous tree species. Oecologia 104, 24-30.

Reich,PB; Tjoelker,MG; Walters,MB; Vanderklein,DW; Buschena,C (1998b): Close association of RGR, leaf and root morphology, seed mass and shade tolerance in seedlings of nine boreal tree species grown in high and low light. Functional Ecology 12, 327-338.

Reich,PB; Uhl,C; Walters,MB; Ellsworth,DS (1991a): Leaf lifespan as a determinant of leaf structure and function among 23 tree species in Amazonian forest communities. Oecologia 86, 16-24.

Reich,PB; Walters,MB (1994): Photosynthesis-nitrogen relations in Amazonian tree species.  II. Variation in nitrogen vis-a-vis specific leaf area influences mass- and area-based expressions. Oecologia 97, 73-81.

Reich,PB; Walters,MB; Ellsworth,DS (1991b): Leaf age and season influence the relationship between leaf nitrogen, leaf mass per area, and photosynthesis in maple and oak trees. Plant, Cell, and Environment 14, 251-259.

Reich,PB; Walters,MB; Ellsworth,DS (1992): Leaf life-span in relation to leaf, plant, and stand characteristics among diverse ecosystems. Ecol. Monogr. 62, 365-392.

Reich,PB; Walters,MB; Ellsworth,DS (1997): From tropics to tundra: Global convergence in plant functioning. Proceeding of the National Academy of Sciences 94, 13730-13734.

Reich,PB; Walters,MB; Ellsworth,DS; Uhl,C (1994): Photosynthesis-nitrogen relations in Amazonian tree species. I. Patterns among species and communities. Oecologia 97, 62-72.

Reich,PB; Walters,MB; Ellsworth,DS; Vose,JM; Volin,JC; Gresham,c; Bowman,WD (1998c): Relationships of leaf dark respiration to leaf nitrogen, specific leaf area and leaf life-span: A test across biomes and functional groups. Oecologia 114, 471-482.
 
Reich,PB; Walters,MB; Tjoelker,MG; Vanderklein,D; Buschena,C (1998d): Photosynthesis and respiration rates depend on leaf and root morphology and nitrogen concentration in nine boreal tree species differing in relative growth rate. Functional Ecology 12, 395-405.

Schulze,E-D; Kelliher,FM; Korner,C; Lloyd,J; Leuning,R (1994): Relationships among maximal stomatal conductance, ecosystem surface conductance, carbon assimilation rate, and plant nitrogen nutrition: A global ecology scaling exercise. Annu. Rev. Ecol. Syst. 25, 629-660.

Sharkey,TD (1985): O2-insensitive photosynthesis in C3 plants. Its occurence and a possible explanation. Plant Physiol. 78, 71-

Small,E (1972): Photosynthetic rates in relation to nitogen recycling as an adaptation to nutrient deficiency in peat bog plants. Canadian Journal of Botany 50, 2227-2233.

Stenberg,P; DeLucia,ED; Schoettle,AW; Smolander,H (1995): Photosynthetic light capture and processing fom cell to canopy. In: Resource Physiology of Conifers:Acquisition, Allocation, and Utilization. 1st ed. Vol. 1. (Eds: Smith,WK; Hinckley,TM) Academic Press, San Diego, 3-8.

Terashima,I; Hikosaka,K (1995): Comparative ecophysiology of leaf and canopy photosynthesis. Plant, Cell, and Environment 18, 1111-1128.

Williams,K; Field,CB; Mooney,HA (1989): Relationships among leaf construction cost, leaf longevity, and light environment in rain-forest plants of the genus Piper. Amer. Natur. 133, No 2, 198-211.