Pugnaire F.I. Valladares F. Functional Plant Ecology

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RESPONSES TO SPATIAL HETEROGENEITY

Photosynthesis and Growth

At the most basic level, spatial heterogeneity in light creates variation in the resources

available and hence in photosynthesis and growth. Because light is highly variable but is

often the most limiting resource in forest understories, correlations between light availability,

photosynthetic parameters, and seedling growth have been demonstrated in many species

(Montgomery and Chazdon 2002, Delagrange et al. 2004, Pearcy et al. 2004). Growth of

understory saplings of two shade-tolerant Hawaiian tree species was highly correlated with

spatial variation in the mean annual potential minutes of sunflecks received as estimated from

fisheye photographs (Pearcy 1983). Similar results have been obtained with understory

saplings in Costa Rica (Oberbauer et al. 1988) and oak seedlings in Japan (Washitani and

Tang 1991). However, spatial heterogeneity in growth is not always correlated with estimates

of sunfleck availability, and in some cases diffuse light availability has been a better predictor

of growth (Tang et al. 1992). Pfitsch and Pearcy (1992) found no correlation between

estimates of sunfleck light availability and growth of the redwood forest understory herb,

Adenocaulon bicolor. Variation in daily carbon gain and in the proportion of the annual

carbon gain contributed by photosynthetic utilization of sunflecks was, however, highly

correlated with the variation in sunfleck availability (Pearcy and Pfitsch 1991). Moreover,

removal of sunflecks with shadow bands designed to block sunfleck transmission along the

solar track but pass most of the diffuse PFD, significantly reduced growth and reproduction

(Pfitsch and Pearcy 1992). Thus, there is no doubt that sunfleck utilization was important to

these plants but other limitations may have prevented translation of the spatial variation in

sunfleck PFD into spatial variation in growth. There is evidence for only minor losses of

carbon gain due to photoinhibition in sunflecks (Pearcy 1994) so other factors such as

drought stress and increased competition in the brighter microsites need to be considered.

Plasticity of the Photosynthetic Apparatus in Response to Spatial Heterogeneity

One of the most universal responses to increased light availability is a plastic response of leaf

photosynthetic properties that results in development of sun leaves that have higher photo-

synthetic capacities per unit area (Amax

area

), greater leaf thickness, and a greater leaf mass

per unit leaf area (LMA). The plasticity expressed by different species in different growth

situations varies widely, ranging from 1.25- to a 3-fold or in a few cases a 5-fold difference in

Amax

area

between sun and shade environments (Bjo

rkman 1981, Pearcy and Sims 1994,

Chazdon et al. 1996, Strauss-Debenedetti and Bazzaz 1996, Huante and Rincon 1998). The

plasticity of Amax

area

can be examined either in terms of the relative change in photosynthetic

rates achieved under light-saturating conditions, or in terms of the range of light environ-

ments over which this plasticity is expressed. Most studies have focused on the former by

comparing plants grown in low- and high-light environments designed to mimic shade and at

least partial sun environments. These are useful for comparing the response to environments,

either simulated or natural, such as a gap and understory but because of the nonlinear

response of most phenotypic traits and the potential for combining acclamatory and inhibi-

tory responses in a stressful environment, they are usually not satisfactory in identifying

species differences in plasticity related to their regeneration niche. When compared in this

way, fast-growing early successional species favoring high-light environments seem to exhibit

greater plasticity of Amax

area

, as compared with more slowly growing, shade-tolerant later

successional shrub and tree species (Strauss-Debenedetti and Bazzaz 1996, Yamashita et al.

2000). Some care is required in interpreting plasticity since the response to the high-light

environment may be a mixture of acclimation and photoinhibition with the latter acting to

reduce Amax

area

(Mulkey and Pearcy 1992). In addition, extremely shaded light environments

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220 Functional Plant Ecology

may interfere with the leaf development of shade-intolerant species, reducing their Amax

area

The way to avoid this problem is to examine photosynthetic responses over multiple light

environments but this has been done in only a few studies (Sims and Pearcy 1989, Valladares

et al. 2000, Muraoka et al. 2003). An interesting approach is to study transplanted seedlings along

light gradient such as across a forest edge in a gap forest to pasture transition, giving a wide range

of light environments (Chazdon 1992, Montgomery 2004). In general, results obtained from

comparisons across multiple environments reveal a strong dependence of Amax

area

on the

daily light availability up to moderate daily PFDs but little further increase. For example,

Montgomery (2004) found that most growth and photosynthetic traits exhibited nonlinear

responses to light availability with the greatest changes between 0.5% and 20% canopy

transmittance of diffuse light with little additional change at higher canopy transmittances.

Given the interacting effects of leaf development, acclimation, and photoinhibition, the

range of light environments over which plasticity is expressed can differ between species, and

may be as important ecologically as the actual change in Amax

area

itself. Sims and Pearcy

(1989) compared the shade-tolerant, rain-forest herb, Alocasia macrorrhiza to the crop

species, Colocasia esculenta in five different light environments ranging from deep shade to

50% of full sun. Both exhibited a 2.2-fold difference in Amax

area

but the range of light

environments over which this was expressed was higher in Colocasia than in Alocasia.

Comparisons of 16 gap-dependent and shade-tolerant Psychotria species across three light

environments from deep shade to 25% of full sun reveals the diversity of responses that can

occur (Figure 7.2). Overall, the plasticity of Amax

area

differed little among the species but the

responses to the changes in light environments contrasted markedly. Most species exhibited

MAR

BRA

GRC

PUB

EME

HOR

MIC

IPE

CHA

ACU

GRD

TEN

PSY

RAC

PIT

LIM

024

Growth light environment

(mol photons m

−2

day

−1

)

Photosynthetic capacity

(µmol m

−2

−1

)

6810

FIGURE 7.2 Response of photosynthetic capacity (Amax) of 16 Psychotria species to growth in three

different light environments simulating understory shade to gap conditions. The abbreviations on the

right side are for the different species and are ordered identically to the symbols shown for the highest

light environment on the right side. The abbreviations are: MAR, Psychotria marginata; BRA, Psycho-

tria brachiata; GRC, Psychotria graciflora; PUB, Psychotria pubescens; EME, Psychotria emetica; HOR,

Psychotria horizontalis; MIC, Psychotria micrantha; IPE, Psychotria ipecacuanha; LIM, Psychotria

limonensis; CHA, Psychotria chagrensis; ACU, Psychotria acuminata; GRD, Psychotria granidensis,

TEN, Psychotria tenuifolia, PSY, Psychotria psychotrifolia; RAC, Psychotria racemosa; PIT. Psychotria

pittieri. The abbreviations in boldface are for gap-dependent species and show that there is no relation-

ship between gap versus understory species and plasticity of photosynthetic capacity. Each data point is

the mean of at least three determinations on different plants. (Adapted from Valladares, F., Wright, S.J.,

Lasso, E., Kitajima, K., and Pearcy, R.W., Ecology, 81, 1925, 2000. With permission.)

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Responses of Plants to Heterogeneous Light Environments 221

the largest increase in Amax

area

between the low and the intermediate light environments.

Some species exhibited a moderate increase between the intermediate and the high-light

environments, others no increase and still others exhibited a decline in Amax

area

from the

intermediate to the high-light environment. These responses of Amax

area

were not correlated

with habitat requirement (gap-dependent vs. understory) of the species, though an overall

measure of plasticity integrating both physiological and morphological characters showed

that gap-dependent species had greater plasticity. Of course Amax

area

is only one of a suite of

characters, and changes in leaf angle and so on may function to reduce the actual range of

incident PFD experienced by the plant to avoid conditions that may cause photoinhibition.

Indeed the PFD on the leaf surfaces is often close to the PFD that is just saturating for

photosynthesis even though the incident PFD on a horizontal surface is much higher. It

would be unrealistic to expect that increasing the PFD would result in a further increase in

Amax

area

. Indeed, the more common result may be photoinhibition.

Only a few studies have examined the plasticity of the photosynthetic apparatus to the

spatial heterogeneity of light environments in the field. Chazdon (1992) found that Amax

area

of an early successionial shrub, Piper sancti-felicis, was closely related to light availability

along transects across natural gaps. A later successional congener, Piper arieianum, exhibited

a weaker association of Amax

area

with light availability, possibly because of a greater

susceptibility to photoinhibition in the gap center (Figure 7.3). Comparisons of a habitat

P. sancti-felicis

P. arieianum

51015

Percent of full sunlight

Distance from west

ap ed

e (m)

Amax (µmol CO

−2

−1

)

10 15

FIGURE 7.3 Gradients of light (open circles) and Amax (closed circles) of seedling of the gap species,

Piper sancti-felicis (top), and the understory species, P. arieanum (bottom) across a small gap. Photo-

synthetic capacity tracks the light environment much better in the gap-dependent species than in the

understory species. (Adapted from Chazdon, R.L., Oecologia, 92, 586, 1992. With Permission.)

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222 Functional Plant Ecology

specialist, the gap-dependent pioneer species, Piper auritum, with a habitat generalist species

with respect to light, Piper hispidum, revealed similar responses of Amax

area

to light avail-

ability but less sensitivity of dark respiration and LMA to light in the specialist species.

Although the net result was similar the two species may differ in the mode of acclimation.

Within the narrower range of light environments in the understory, Chazdon and Field (1987)

found no correlation between microsite light availability and Amax

area

in response to micro-

site variation in the understory but did find increasing Amax

area

with increasing light

availability in gap environments. These results suggest that below a lower threshold PFD

no further adjustments in photosynthetic capacity occur.

Sunflecks are a primary source of heterogeneity in daily PFD in the understory, but these

are certainly too unpredictable for any advantage in daily carbon gain to accrue from

adjustment of Amax

area

. Sims and Pearcy (1993) found no differences in Amax

area

among

Alocasia macrorrhiza plants grown under either short or long sunflecks or constant PFD

environments where each environment had identical daily PFDs. Pearcy and Pfitsch (1991)

found that Amax

area

, LMA, and leaf N per unit area of the A. bicolor plants grown under

shadow bands were all positively correlated with diffuse PFD levels. However, no correlation

between these measures and either total PFD of sunfleck PFD was found for the adjacent

control plants that received sunflecks. A filtering mechanism that ignored the unpredictable

component of variation in daily PFD associated with sunflecks but allowed response to the

much less variable but more predictable diffuse component would explain these results.

Maximizing Photosynthesis in High Light

Maximizing photosynthetic performance in high light requires investment in the carboxyla-

tion and electron transport capacity necessary to support high photosynthetic rates coupled

with a sufficiently conductive pathway for CO

diffusion through the stomata and to the site

of carboxylation in the chloroplasts. Growth in high versus low light has been shown to result

in increases in activities (concentrations) per unit area of the primary carboxylating enzyme

ribulose-1,5 bisphosphate carboxylase=oxygenase (Rubisco), Photosystem II (PSII) electron

transport capacity, the electron carrier, cytochrome f, and chloroplast coupling factor that is

involved in ATP synthesis (Bjo

rkman 1981, Anderson and Osmond 1987). It is likely that

nearly all components in the photosynthetic carbon reduction cycle (PCRC) and electron

transport must increase in a coordinated manner to maintain a balance between capacities of

each component step. Indeed, acclimation seems to result in at most only a small increase in

the ratio of electron transport to carboxylation capacity (Sims and Pearcy 1989, Thompson

et al. 1992, Wullschleger 1993). Stomatal conductance must also increase to maintain a

balance between the capacity for supply and for utilization of CO

. Since internal diffusion

limitations across cell walls and membranes to the Rubisco in the chloroplast are significant

(Evans and Von Caemmerer 1996) these must also be adjusted to accommodate sufficient

transport as photosynthetic capacity is increased.

Insight into the causes of the plasticity in photosynthetic capacity can be gained by

comparing differences in photosynthetic capacities calculated on a per unit leaf area basis

(Amax

area

) with those calculated at per unit leaf mass basis (Amax

mass

). Across ecologically

and geographically broad species comparisons of high light-adapted species, thinner leaves

with lower LMA have higher Amax

mass

than thicker, high LMA leaves (Reich et al. 1997).

Across species and especially across life forms much of the difference in Amax

mass

is clearly

due to genetically determined differences in concentrations of photosynthetic machinery per

unit mass. From gas exchange analysis, Rubisco carboxylation capacity and electron trans-

port capacity are higher in the thin-leaved species and the stomatal and liquid phase

conductances to CO

also increase concurrently. The positive relationship between Amax

mass

and leaf nitrogen per unit mass is also consistent with a greater investment per unit mass in

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Responses of Plants to Heterogeneous Light Environments 223

photosynthetic enzymes. Liquid phase diffusion limitations may also be important. Sclero-

phylous leaves that are characterized by low Amax

area

are typically hypostomatous, have

been shown to have a lower CO

transfer conductance both through the intercellular air

pathway and across the cell wall and liquid phase to the site of carboxylation than mesophytic

leaves (Parkhurst and Mott 1990, Evans and Von Caemmerer 1996). Investment in thick cell

walls characteristic of sclerophylous leaves dilutes the photosynthetic machinery resulting in

low Amax

mass

. Amphistomaty serves to overcome limitations to intercellular airspace diffu-

sion in high photosynthetic capacity leaves by providing a pathway through both epidermi

(Mott et al. 1982, Parkhurst and Mott 1990).

For light acclimation, the picture that emerges is somewhat different in that leaves that

develop following a transfer of the plant from low to high light have higher LMA, are thicker,

and have a higher Amax

area

and g

than leaves that develop in the shade before the transfer.

However, in many, perhaps most, species there is little or no change in Amax

mass

despite the

change in leaf thickness. An increase in leaf thickness occurs because leaves developing in the

sun typically have two layers of palisade, or longer palisade cells (Kamaluddin and Grace

1992), above a spongy mesophyll, whereas those developing in the shade have only a loosely

organized and relatively undifferentiated and thin mesophyll (Chabot and Chabot 1977,

Bjo

rkman 1981). This is consistent with a constant amount of photosynthetic machinery

per unit mass but with the greater LMA in sun leaves resulting in a greater concentration of

photosynthetic machinery per unit area. Similarly, significant relationships between Amax

area

per unit area and N per unit area have been commonly found in comparisons of plants grown

in the sun and the shade (Seemann et al. 1987, Evans 1989b, Hikosaka and Terashima 1996),

whereas there is no significant correlation between assimilation rates and N on a mass basis

for most species. Indeed, for many species, increased leaf thickness resulting in increased cell

and chloroplast volume per unit leaf area may be the only mechanism involved in the

observed plasticity of Amax

area

since Amax

mass

remains nearly constant across light envir-

onments (Ellsworth and Reich 1992, Sims and Pearcy 1992). Since the leaf anatomy is

largely specified early in leaf development (Sims and Pearcy 1992), mostly or fully devel-

oped leaves of many species show little or no capacity for adjusting Amax

area

(Mulkey and

Pearcy 1992, Sims and Pearcy 1992, Newell et al. 1993, Oguchi et al. 2005). Some species,

however, can increase their Amax

area

moderately even in fully developed leaves (Chazdon

and Kaufmann 1993, Kursar and Coley 1999, Yamashita et al. 2000). Species that can

respond may do so primarily by increases in chloroplast numbers or volume that fill cell

wall locations unoccupied by chloroplasts when the leaf developed in the shade. On the

other hand, species that are unable to respond may lack unoccupied locations for chloro-

plasts (Oguchi et al. 2003, 2005).

High-light environments, in addition to supporting higher photosynthetic carbon gains,

also present circumstances where excess light may be potentially damaging. Moreover, this

photoinhibition may be exacerbated by the co-occurrence of high temperatures and water

stress (Mulkey and Pearcy 1992, Koniger et al. 1998). Upper canopy leaves in tropical forests,

and also leaves in treefall gaps can reach temperatures 108C above air temperature (Koniger

et al. 1995, Niinemets and Valladares 2004). On the other hand, lower canopy leaves are

usually near air temperatures. Thus, morphological and biochemical mechanisms that min-

imize photoinhibitory damage are important in acclimation to high light. Steep leaf angles

and preferential orientation of leaves function to minimize the potential for photoinhibition

yet maintain sufficient fluxes to also maximize photosynthetic carbon gain (Ehleringer and

Forseth 1980, Ludlow and Bjo

rkman 1984, Gamon and Pearcy 1989). Within plant crowns,

upper leaves often have steep leaf angles, decreasing the receipt of solar radiation at midday,

whereas lower leaves have shallower leaf angles to maximize light capture (Valladares 1999).

In addition to affording structural photoprotection in the upper canopy, changes in leaf

angles decrease vertical heterogeneity in intercepted light.

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224 Functional Plant Ecology

Structural photoprotection is also accompanied by biochemical photoprotection involv-

ing down-regulation of PSII via the xanthophyll cycle where excess energy is dissipated by

heat (Demmig-Adams and Adams 1992b, 1996, 2000). Sun leaves possess greater total pool

sizes of xanthophyll-cycle pigments and a greater capacity for rapid conversion of violox-

anthin to antheroxanthin and zeaxanthin that invokes this photoprotection (Thayer and

Bjo

rkman 1990, Demmig-Adams and Adams 1992a, 1994). In addition, sun leaves have a

greater capacity for scavenging of active oxygen free radicals that can cause photodamage

(Grace and Logan 1996). When shade leaves are exposed to PFD in excess of the capacity of

these mechanisms, photodamage to PSII may occur, requiring operation of a PSII repair

cycle for recovery (Geiken et al. 1992, Oquist et al. 1992, Anderson et al. 1995).

Maximizing Photosynthesis in Shade

Maximizing leaf photosynthetic performance at the low PFDs inherent in shaded, diffuse-

light conditions requires (1) maximizing light absorptance, (2) maximizing the quantum yield

with which this light is used for CO

assimilation, and (3) minimizing respiratory losses.

Careful comparisons under conditions where photorespiration is suppressed (low O

or high

partial pressures) have unequivocally established that there are no intrinsic differences in

quantum yields between C

species adapted to sun and shade habitats or, provided that no

stress effects interfere, among leaves on plants grown in high and low light (Bjo

rkman and

Demmig 1987, Long et al. 1993, Singsaas 2001). The observed quantum yields are consistent

to those derived from stoichiometric requirements for production of the ATP and NADPH

necessary for carbon metabolism, small inefficiencies in energy transfer inherent within the

chlorophyll antennae and reaction centers, and energy use for other processes such as nitrate

reduction. Thus, there is essentially no scope for further improvements in shade as compared

to sun leaves. Photorespiratory losses under normal atmospheric concentrations reduce the

achieved quantum yields under natural conditions, but this is slightly different for sun and

shade plants. Recently, it has been reported that quantum yields are reduced in extremely low

light possibly because of insufficient buildup of the transthylakoid proton gradient required for

ATP regeneration (Timm et al. 2002, Kirschbaum et al. 2004). Since quantum yields were

greater than 85% restored by PFDs as low as 5 mmol m

2

1

, the loss of quantum yield would

have an effect on carbon gain only early or late in the day, or only in the shadiest microsites.

Quantum yields are frequently reduced because of photoinhibition, especially when high

light is coupled with high leaf temperatures, water stress, or low nitrogen nutrition (Bjo

rkman

et al. 1981, Bjo

rkman and Powles 1984, Ferrar and Osmond 1986, Mulkey and Pearcy 1992,

Koniger et al. 1998). Shade leaves are more susceptible to photoinhibition than sun leaves in

this regard and observed differences in quantum yields may often be due to the occurrence of

these other environmental factors and their interaction with high PFD. On the other hand,

higher CO

concentrations in the understory and the high values of intercellular to ambient

pressures (c

) characteristically observed under diffuse light conditions can enhance

quantum yields for CO

uptake by 10%–20% due to reduced photorespiration (Pfitsch and

Pearcy 1989a, DeLucia and Thomas 2000, Singsaas et al. 2000). This enhancement could be

important under the conditions of rising atmospheric CO

in allowing plants to occur in

shadier microsites than would be the case under current CO

concentrations.

Comparisons across many species also reveal no consistent differences in leaf absorptance

or chlorophyll (Chl) concentration per unit leaf area between sun and shade leaves (Bjo

rkman

1981). Chl concentrations per unit area are typically sufficient to absorb 85%–92% of the

incident photosynthetically active radiation with the remainder lost to either reflection or

transmission. The lower LMA of shade leaves means that to maintain Chl per unit area

constant there has to be an increased investment in Chl per unit mass. Although shade leaves

in particular could benefit in terms of increased photosynthesis from increased Chl per unit

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Responses of Plants to Heterogeneous Light Environments 225

area and hence leaf absorptance, the strongly diminishing returns of further investment in

Chl–protein complexes required to affect a significant change in light capture may preclude it.

A doubling of the Chl concentrations is required to increase leaf absorptance by just 5%–6%

from the levels given earlier. Although there are only 4 mmol N in a mol of Chl, the associated

proteins in the Chl–protein complexes contain 21–79 mmol N mol

1

Chl (Evans 1986, 1989a).

Chlorophyll a=b ratios are much lower in shade than sun leaves and it was suggested that this

may represent a mechanism for increasing absorption in the 640–660 nm wavelength range

where PFD in the understory is somewhat greater than that at longer wavelengths where Chl

in the overstory canopy has its maximum absorption. The advantage, however, may lie more

in a significant savings of N since Chl b is part of the light-harvesting chlorophyll–protein

complex II (LHCII), which contains only 25 mmol N mol

1

Chl, whereas Chl a in PSII

represents an investment of 83 mmol N mol

1

Chl (Evans 1986). The lower Chl a=b ratio

results from increased LHCII per unit leaf area coupled with decreased concentrations of the

PSII core complex, which contains only Chl a. Since PSII complexes contain more N, the shift

to more LHCII while maintaining total Chl per unit leaf area constant results in a signifi-

cantly greater light capture per unit N invested. This savings is possible in shade, but not sun

leaves because high capacities of PSII electron transport are needed in the high light.

Acclimation of Dark Respiration

To maintain a positive carbon return, gross assimilation rates must clearly exceed respiration

rates. It is now widely documented that one of the most important differences between sun

and shade leaves are the much lower respiration rates of the latter (Grime 1966, Bjo

rkman

1981). Leaf respiration itself and especially the mechanisms responsible for lower rates in

shade leaves are not well understood. Respiration rates may be affected by the capacity of the

respiratory pathways, substrate concentrations, rates of energy and reductant demand, and

the extent of alternative pathway engagement. In addition, mitochondrial respiration is

substantially inhibited by light at PFDs as low as 3 mmol m

2

1

(Atkin et al. 1998, 2000).

Thus, measurements done in the dark, the commonly used method for estimating respiration,

rather than the more complex procedure of Laisk (1977), must be corrected in models

exploring carbon balance in understory plants.

Mitochondrial respiration occurs in response to growth and maintenance processes. Since

the low available light severely limits carbon gain and growth in the shade, respiration rates of

the leaves of shade plants are correspondingly low, which is critical for maintaining a positive

carbon balance in understory light regimes. The observed respiration rates of sun and shade

plants reflect mostly the differing resource supplies and demands. Respiration rates appear

to be differently regulated in sun and shade species (Noguchi et al. 1997, Noguchi and

Terashima 1997). In the high-light species, Spinacia oleracea, respiration rates were limited

by the carbohydrate supply in the leaves, whereas in the shade-adapted species, Alocasia

odorata, they were limited by a low demand for ATP due to its slow growth rate. Transfer

from high to low or from low to high light typically invokes a corresponding decrease or

increase in dark respiration rates over the following 4–6 days (Sims and Pearcy 1992, Noguchi

et al. 2001b). In shade plants such as Alocasia odora, feeding experiments involving either

carbohydrates or respiratory inhibitors show that this decline in respiration on transfer

from high to low light occurs because of the reduced demand for ATP. Conversely, in high

light, more respiration may be needed for repair of PSII photodamage or for the greater

phloem loading as growth accelerates and biosynthesizes. Overall, the maintenance costs

of the photosynthetic apparatus are lower in shade than those in high light-acclimated

leaves because of the lower soluble protein levels (Noguchi et al. 2001a) and likely lower

costs for repair of photodamage. However, even in high light-acclimated leaves, maintenance

respiration relative to photosynthetic capacity still appears to be a rather low cost measured

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226 Functional Plant Ecology

relative to photosynthetic capacity and perhaps not much different between shade- and

sun-acclimated leaves (Sims and Pearcy 1992).

Of more importance than maintenance respiration to the carbon balance of leaves and the

payback time for a positive return on investment may be the construction costs, which occur

principally early in the leaf ’s development, but which must be paid back over the leaf lifetime.

On a per unit area basis, sun leaves are more expensive to construct because they are thicker

and have higher per unit area concentrations of photosynthetic enzymes. On a per unit mass

basis there is on average only a slightly greater (3%) construction cost of sun as compared

with shade-acclimated leaves (Poorter et al. 2006). Construction costs depend on the com-

position of the leaf and vary depending on the amounts of more costly, reduced compounds

such as soluble phenolics, lipids, proteins, and lignin as compared with carbohydrates. Sun

leaves can recover construction costs within a few days, whereas shade leaves may require

60–150 or more days, depending on the light environment (Chabot and Hicks 1982, Jurik and

Chabot 1986, Sims and Pearcy 1992).

Trade-Offs and Optimality in Sun Shade Acclimation

Modeling approaches have been used that explore the trade-offs involved in acclimation with

respect to whether they maximize the return on investment in a given light environment. At

the leaf level, one trade-off is how a given amount of biomass should be invested in either

increasing the area of the leaf, thereby enhancing light capture, or in increasing leaf thickness

thereby increasing the Amax

area

of the leaf. A second trade-off involves how N should be

partitioned within the photosynthetic apparatus in a given light environment to maximize

photosynthesis. This involves a trade-off between investment of N to maximize photo-

synthetic rate in high light versus investment in pigment–protein complexes that increase

the slope of the light response curve in low light (Evans 1989b). Several studies have shown

that nitrogen partitioning between light capture components (Chl-proteins) and compo-

nents that increase photosynthetic capacity (Rubisco and electron transport carrier com-

ponents) change with acclimation in a way that almost maximizes photosynthesis (Evans

1993, Hikosaka and Terashima 1995, 1996, Niinemets et al. 1998b). Moreover, daily carbon

gain is quite sensitive to the changes in allocation observed in high versus low light-acclimated

leaves, each with 20%–30% lower daily carbon gain in the light environment opposite to the

one that they were grown in (Hikosaka and Terashima 1996). Central to these optimizations

are first that light absorption is a hyperbolic function of chlorophyll content in agreement

with observed changes (Gabrielsen 1948) and second that relatively small changes in the

fraction of N allocated to pigment–protein complexes have a large effect on light absorption.

Comparisons of the assimilation rates per unit leaf area at the simulated optimum partition-

ing to the actual measured assimilation rates revealed that the latter tracked the former quite

closely with deviations only in the highest and lowest light environments. The changes for

shade and sun species did not track in the highest and lowest light environments, respectively.

Thus, nearly optimal partitioning could be maintained over a range of light environments, but

this range differed between shade and sun species.

Changes in LMA mediate the other trade-off in that a given amount of biomass invested

in a leaf can either be spread over a small area increasing its Amax

area

or over a large area

increasing its light capture. Sims et al. (Pearcy and Sims 1994, Sims et al. 1994) modeled the

sensitivity of whole-plant growth rate to changes in Amax

area

and LMA in Alocasia macro-

rrhiza. When just LMA was varied RGR was more sensitive to changes in LMA in the low-

light environment than in the high-light environment. Conversely, when just Amax

area

was

varied RGR was much less sensitive to changes in the low-light environment as compared

with the high-light environment. When LMA and photosynthetic capacity were varied

simultaneously, as occurs in acclimation, then RGR was much more sensitive in low as

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Responses of Plants to Heterogeneous Light Environments 227

compared with high light. These simulations emphasize the central role of changes in LMA in

acclimation to sun and shade and especially in improving performance in low light. This is

further emphasized in simulations where changes in N partitioning and in LMA characteristic

of acclimation were compared (Evans and Poorter 2001). This comparison revealed that daily

photosynthesis per unit dry mass is far more sensitive to changes in LMA than to changes in

allocation of N.

PLASTICITY OF WHOLE-PLANT RESPONSES

Integration of the role of photosynthetic plasticity in enhancing plant function in hetero-

geneous light regimes requires an understanding of how leaf photosynthetic rates interact

with and are determined by allocation patterns at the whole-plant level. Since the carbon

content of biomass is nearly constant, growth and whole-plant photosynthesis are indeed

closely linked by the conversion efficiency of fixed carbon into biomass (Dutton et al. 1988).

Whole-plant photosynthesis is simply the photosynthetic rate of the leaves integrated over the

leaf area. Of course, it is necessary to take into account that leaves are in different light

microenvironments within the crown and, because of acclimation and aging phenomena, may

have different capacities to use this light. Moreover, the carbon losses via respiration at the

whole-plant level must be subtracted to arrive at a whole-plant carbon balance.

Enhanced whole-plant photosynthesis can therefore be obtained either by increasing the

photosynthetic rate per unit area under the prevailing conditions, or by increasing the leaf

area per plant. An important linkage in this process is the LMA since this determines how

much leaf area is produced for a given investment of biomass in leaves. Most studies have

found that the leaf weight ratio (LWR: mass of leaves per unit mass of plant) tends to be

higher in sun as compared with shade-grown plants but the differences are usually rather

small (Bjo

rkman 1981, Poorter and Nagel 2000). Instead, shade-grown plants invest more in

stems and less in roots with little change in total leaf area (Reich et al. 1998). Greater

investment in stems may be helpful in minimizing self-shading. Although the proportional

biomass investment in leaves tends not to vary much with sun-shade acclimation, shade-

grown plants typically have a much larger leaf area ratio (LAR: area of leaves per unit mass

of plant) than sun plants because of the large differences in LMA. Since, as discussed earlier,

LMA is also a determinant of Amax

area

, it clearly mediates a trade-off between lower

Amax

area

and greater leaf area for light capture in the shade, versus higher Amax

area

but

less leaf area in the sun. The result in the shade is a large advantage in whole-plant carbon

gain for the shade plant (Figure 7.4). Perhaps counterintuitively, experiments and simulations

have shown no carbon gain advantage per unit biomass invested for the sun plant phenotype

in high light since the reduced leaf area per plant more than offsets the advantage accrued due

to the higher Amax

area

(Sims and Pearcy 1994, Sims et al. 1994). Indeed, shade-acclimated

sunflower plants have been shown to have higher relative growth rates immediately after

transfer to high light than do plants grown continuously in the high-light environment (Hiroi

and Monsi 1963). Subsequent acclimation of the shade plant to the sun environment therefore

actually causes the RGR to decrease. This does not mean that sun leaves provide no

advantage in high light, especially over the long term, since they may well contribute to a

greater stress resistance and greater water and nitrogen use efficiency.

RESPONSES TO WITHIN-CROWN SPATIAL HETEROGENEITY

Within a plant crown, growth itself generates a heterogeneous light environment as younger

branches and leaves overtop and shade lower branches and older leaves. This gradient has

been studied in tree canopies (Niinemets et al. 1998b, Ellsworth and Reich 1993), herbaceous

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228 Functional Plant Ecology

vegetation (Anten et al. 1995, Hirose et al. 1988), and crops (Gutschick and Wiegel 1988) and

occurs both in closed canopies and in the crowns of isolated plants (c.f. Caldwell et al. 1986).

In all, the gradient in light is primarily a function of the cumulative leaf area index and the

architecture of the leaf and branch elements that controls the aggregation, inclination, and

self-shading of leaves within and between shoots. Response to this highly dynamic gradient

involves both senescence of older, more shaded leaves with reallocation of resources to

the newly developing leaves in the higher-light environments as well as acclimation to the

changed light environment. The modular nature of plants and the semiautonomy of these

modules confers great flexibility to plants in responding to fine-grained differences in light

availability (de Kroon et al. 2005).

Studies of the consequences of light attenuation within plant crowns have focused on the

question of how resources, in particular nitrogen and also LMA, should be distributed

between leaves at different positions in the crown to maximize photosynthesis. Optimal N

use occurs when canopy photosynthesis is maximized for a given whole-canopy N content

(Field 1983, Hirose and Werger 1987a). Optimal N use demands that more N be partitioned

to the upper leaves located in high light, resulting in a higher Amax

area

of these leaves as

compared with lower leaves in more shaded microenvironments. Differences in LMA have

been shown to be central to this partitioning because of its pivotal role in determining

photosynthetic capacity and N contents in sun and shade leaves. The optimal N distribution

between leaves is the one that results in a gradient of photosynthetic capacity through the

Instantaneous assimilation rate

single leaf

−1

0.3

0.2

0.1

0.0

−0.1

0.4

0.3

0.2

0.1

0.0

0 400 800 1200 1600 0 5 10 15 20 25

−0.1

−2

(a)

(b)

Daily assimilation integral

whole plant

PFD (mol m

−2

day

−1

)

Assimilation (mol m

−2

day

−1

)

Assimilation (µmol m

−2

−1

)

Assimilation (µmol g

−1

)

Assimilation (mol g

−1

day

−1

)

PFD (µmol m

−2

−1

)

FIGURE 7.4 Response of instantaneous assimilation rates to PFD for leaves (a,c) and daily assimilation

rates of whole plants (b,d) of Alocasia macrorrhiza acclimated to sun (open circles) and shade (closed

circles) conditions. The curves for whole plants were obtained by growing individual plants in sun or

shade conditions and then transferring to a whole-plant chamber for gas exchange conditions. Different

daily PFDs were obtained with neutral-density screen and cloth filters under natural sunlight. (Adapted

from Sims, D.A. and Pearcy, R.W., Plant, Cell Environ., 17, 881, 1994. With permission.)

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Responses of Plants to Heterogeneous Light Environments 229