Pugnaire F.I. Valladares F. Functional Plant Ecology

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fact that there are greater induction limitations for the long lightflecks as shown experimen-

tally (Chazdon and Pearcy 1986b) and a greater relative contribution of postlightfleck CO

assimilation for short lightflecks.

Dynamic models are also useful for assessing the role of specific dynamic elements by

selectively modifying the input parameters so that one or more elements become static while

the others remain dynamic (Table 7.1). This is done by changing time constants such that g

or Rubisco light activation or RuBP regeneration light activation, or any combination,

respond instantly to a change in PFD, whereas the other limitations remain dynamic.

Removing the dynamic stomatal limitations alone had a much larger effect than removing

the Rubisco activation limitations. In the latter scenario, Rubisco responds instantaneously

whereas stomata responded slowly, causing c

to decrease and to more strongly limit carbon

gain. Removing the dynamic stomatal limitations caused c

to be higher increasing assimila-

tion (see Figure 7.6). Removing both Rubisco activation and stomatal dynamic limitations

caused assimilation to be nearly the same as predicted by the steady-state model. Finally,

removing all dynamic limitations except for the metabolite pools responsible for postlight-

fleck CO

assimilation gave an identical carbon gain to the steady-state version of the model,

except for the short 5 s lightflecks where carbon gain was increased. Postlightfleck CO

assimilation made no significant contribution to the simulated carbon gain in the understory

because, as discussed earlier, short lightflecks themselves made only a very small contribution

to the available PFD. However, the contributions may be significant or may at least offset

(a)

(b)

(e)

(d)

A, dynamic

(µmol CO

−2

−1

)

A, steady state

(µmol CO

−2

−1

)

1600

1200

800

400

PFD

(µmol photons m

−2

−1

)

6 8 10 12

Time (h)

14 16 18

6 8 10 12

Time (h)

14 16 18

100

0.0

0.2

0.4

0.6

0.8

1.0

(mmol H

O m

−2

−1

)

Rubisco activity

relative

RuBP+R

(µmol m

−2

)

FIGURE 7.8 Simulated daily course of (a) assimilation of an Alocasia macrorrhiza leaf from the dynamic

model of Pearcy et al. (1997) and (b) a steady-state version of the same model under (c) a natural sunfleck

regime in the understory of a Queensland, Australia tropical forest. Additionally, shown are the simulated

daily courses of (d) g

, (e) Rubisco activity and (f) Pool sizes of RuBP and its high-energy precursors.

Model inputs of PFD and the outputs were at 1 s intervals. (From Pearcy, R.W., Chazdon, R.L., Gross,

L.J., and Mott, K.A., Exploitation of Environmental Heterogeniety by Plants: Ecophysiological Processes

above and below Ground, Academic Press, San Diego, CA, 1994. With permission.)

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240 Functional Plant Ecology

some of the induction limitations in other circumstances. Simulations for crop, quaking

aspen, and poplar canopies show that postlightfleck CO

assimilation can contribute to as

much as a 6% enhancement of carbon gain under windy conditions when short sunflecks

make a much more significant contribution (R.W. Pearcy and J. Roden unpublished results).

In the understory, induction limitations predominate and significantly constrain carbon gain

during sunflecks. Of these, dynamic stomatal limitations and the relationships between

stomatal opening and Rubisco activation may be especially important.

Growth Responses to Sunflecks

At the ecological level, sunfleck responses, if they are of significance, should have conse-

quences for the growth of plants. Such experiments are complicated since they require careful

matching of light regimes in terms of the total PFD and differ only in their temporal

variation. Comparisons of RGR for plants in microsites differing in sunfleck light regimes

(Leakey et al. 2003b) are difficult because other factors may also differ. Thus experimental

protocols in greenhouses using shutters to create lightflecks or in growth cabinets (Sims and

Pearcy 1993, Watling et al. 1997) are better for unraveling the growth responses. Adding

lightflecks onto a diffuse light background increases the total PFD, so comparisons back to

assimilation under just the diffuse PFD include both the effects of the greater total PFD as

well as any temporal effects due to the sunflecks. The PFD in the diffuse light regime can be

increased to match that of the lightflecks plus diffuse light. However, in this case, assimilation

is undoubtedly higher in the diffuse light because of the nonlinear nature of the photosyn-

thetic response and because the diffuse light usually falls in the light-dependent part where

PFD is used more efficiently. This approach was used by Watling et al. (1997) who found that

TABLE 7.1

Simulations of Lightfleck Use in Regimes with Either 5 min or 5 s Lightflecks

or for Natural Light Regimes

Conditions

All

Limitations

Stomatal

Limitation

Rubisco

Limitation

Stomatal and

Rubisco

Limitations

Stomatal,

Rubisco, and

FBPase Limitations

5 min lightflecks

22 10 21 10

5 s lightflecks

210 6 12

Understory light regimes

PFD mmol

2

day

1

Percent in

sunflecks

1.28 48 3 1 20 0

0.52 23 7 2 60 0

1.55 59 17 7 15 50

1.18 71 25 8 22 10

Note: Values in the table are percentage differences between a dynamic and a steady-state simulation using the model

of Pearcy et al. (1997). A value of 10, for example, means that dynamic limitations inherent in leaf photosynthetic

responses to lightflecks result in a carbon gain that is 10% less than that predicted by a steady-state model. The model

was initially parameterized for an Alocasia macrorrhiza leaf and then various dynamic limitations were removed.

Either three 5 min lightflecks or one hundred and sixty nine 5 s lightflecks uniformly distributed in an 8.6 h period.

The lightfleck and shade PFDs were 500 and 15 mmol m

2

1

, respectively.

Recorded at 1 s intervals in four sites in the understory of a tropical forest in Queensland Australia. PFD is the daily

total and percent in sunflecks is the percentage of the daily total that was received as sunflecks.

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Responses of Plants to Heterogeneous Light Environments 241

in three of the four species tested, RGR was higher in the constant light than the lightfleck

regime. Addition of lightflecks to a background of low PFD, resulting in additional total

PFD, clearly increased RGR, except in Alocasia macorrhiza where RGR decreased for

unknown reasons. Sims and Pearcy (1993) compared growth of A. macorrhiza under regimes

of (1) long (8 min) but infrequent light flecks, (2) short (6 s) but frequent lightflecks, and (3)

diffuse light only, where all were carefully matched with respect to daily PFD. They found

that relative to the diffuse light only control, RGR was more inhibited under the long than the

short lightfleck regime. This is consistent with the greater expected induction limitation in the

long lightflecks.

Other growth experiments have yielded contrasting results, possibly because of species

differences but also possibly different experimental protocols. Growth of dipterocarp seed-

lings was much greater in a long sunfleck regime created in a small gap than in a short

sunfleck regime in the nearby understory (Leakey et al. 2003b). However, to match the total

daily PFDs, shadecloth was used in the gap, also reducing the peak sunfleck PFD. The

sunflecks therefore differed not only in their duration and maximum PFD, but also in their

dispersion through the day. The experiment clearly shows that different sunfleck regimes have

consequences for growth that can in part be attributed to differences in the dynamics of

assimilation during sunflecks but the contrasting results as compared with those of Sims and

Pearcy (1993) could be explained by any one of several factors.

Sunflecks can also be removed with shadow bands positioned over plants that block the

view of the solar path. Growth of these plants can then be compared with the nearby control

plants that receive sunflecks. This protocol revealed that sunfleck removal caused A. bicolor

plants to decrease in size over 2 years as maintenance costs exceeded carbon supply, indicat-

ing that sunflecks were of great significance to the survival of this species (Pfitsch and Pearcy

1992). The individual pairs of plants were in different microsites receiving different sunfleck

light regimes so that it was also possible to compare growth between the different microsites.

An analysis of covariance, however, revealed no significant relationship between plant

performance and the availability of sunflecks. Although additional sunflecks should increase

carbon gain, competition for nutrients or greater water stress in the brighter microsites may

have limited plant performance. Indeed, many of the characteristics such as the variation in

LMA were better correlated with diffuse PFD than with sunfleck PFD.

RESPONSES TO GAP DYNAMICS

Temporal Nature of Gap Light Regimes

The most studied case of the responses to long-term temporal heterogeneity in light environ-

ments concerns tree-fall gaps in forests (Bazzaz and Carlson 1982, Canham 1989, Canham

et al. 1990, Bazzaz 1991). When a tree falls there is an essentially instantaneous increase in

PFD, followed by a gradual decrease as the gap is filled with new growth. The increase

depends on gap geometry and cloudiness. Therefore, the dynamic response of an understory

plant to the formation of a gap may depend on whether it occurs during a period of cloudy or

clear weather.

Response to the increase in PFD following gap formation has received much more

attention than the response to the much more gradual decrease that occurs as a gap fills.

Gap filling occurs both from the bottom up as plants established in the gap gain height and

from the sides as branches extend out into it. Significant shading of seedlings may develop

within a year or two, whereas at higher levels the gap may not fill for several to many years.

Thus, shading of saplings may be delayed as compared to seedlings. This gradual refilling

stage may be quite important for understory shrubs that establish in gaps but persist and

reproduce in the understory long after that gap has closed. Most tropical forest trees may

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242 Functional Plant Ecology

require multiple gap events to make the transition from understory seedling to sapling to a

canopy tree. Thus just how the photosynthetic apparatus and allocation patterns adjust to the

gradual decrease in PFD as a gap closes could be quite important for persistence.

Dynamic Plasticity of Leaves and Plants to Long-Term Temporal Heterogeneity

Following a gap formation both acclimation of leaves and shifts in allocation to restore a

functional balance at the whole plant level are important mechanisms for responding to the

increased light availability. Kursar and Coley (1999) have identified two modes of acclima-

tion, one where relatively short lived but inexpensive leaves are quickly dropped and replaced

by a canopy of sun leaves. The other is where long lived, expensive leaves are retained and are

only gradually replaced and exhibit moderate acclimation to the increased light. Long-lived

leaves were initially more tolerant of high light stress and exhibited less photoinhibition

measured as the reduced F

values the following morning. These contrasting modes,

which are probably representative of extremes along a spectrum of responses, are indicative

of a trade-off between a capacity to rapidly accelerate growth with increased light availability

and greater stress tolerance.

In terms of responses to gap formation the most revealing and ecologically relevant

experiments are those that follow the dynamics of acclimation following a light increase

(Ferrar and Osmond 1986, Mulkey and Pearcy 1992, Turnbull et al. 1993). These experiments

typically reveal initial reductions in quantum yields and the fluorescence ratio F

indica-

tive of photoinhibition, and usually a reduction of light-saturated photosynthetic rates. This

reduction in F

can last for 1 day to a week or more but if conditions are not too severe,

recovery from photoinhibition occurs. In peas, only a small, 1 day reduction in Amax

occurred before Amax increases rapidly within 4 days to a new, threefold higher steady-

state value (Anderson and Osmond 1987). In the evergreen tropical tree species Bischofia

javanensis, Amax and the chlorophyll fluorescence ratio, F

, remained depressed for

nearly 8 days, and 30 days were required to reach the new steady-state Amax (Kamaluddin

and Grace 1992). In the temperate vine, Hedera helix, 45 days were required to complete the

acclimation process (Bauer and Thoni 1988). Low nitrogen status exacerbates the initial

photoinhibitory reduction in Amax and slows or prevents full recovery when shade-grown

plants are transferred to high light (Ferrar and Osmond 1986). High-leaf temperature also

strongly interacts with the PFD level, causing a greater inhibition and slower recovery.

If the extant leaves are capable of acclimation, a further slow increase in Amax occurs. In

mature leaves incapable of acclimation, an initial decline in photosynthetic rates occurs

followed by at least a partial recovery if conditions are not too severe. New leaves then

develop with a higher photosynthetic capacity. Ultimately acclimation at the whole-plant

level is complete when there has been a complete turnover of the leaves and adjustments in

LAR and root=shoot ratios have occurred. Depending on the species involved and its leaf

longevity and production rates, full acclimation could take weeks to years.

A key to the initial response to gap formation is the dynamic interaction between

acclimation and photoinhibition. As shown in Figure 7.9, exposure of shade-grown Alocasia

macrorrhiza plants to 2 h of direct sunlight superimposed on a shade-light background

resulted in a strong initial reduction in F

and Amax followed by an almost complete

recovery of F

and only a partial recovery of Amax in 5–10 days (Mulkey and Pearcy

1992). The recovery during successive days with the same light treatment suggests develop-

ment of an increased capacity for photoprotection. Leaves that developed under this gap

simulation were completely resistant to photoinhibition and had a higher Amax. Thus

complete acclimation required replacement of all the leaves, requiring in this species 60–80

days. Although the preexisting leaves had a reduced photosynthetic capacity as compared

with later-developing leaves, they still provided substantial carbon gain because of the high

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Responses of Plants to Heterogeneous Light Environments 243

light. Thus, protecting them through rapid acclimation of photoprotective mechanisms may

be quite important for maintaining a carbon supply for growth of the new leaves. In this

experiment, a strong interaction between high light and high leaf temperatures was found that

greatly increased photoinhibition and delayed the recovery. This interaction is undoubtedly

quite important in natural gap formation since leaf temperatures in gaps with bright sunlight

can be 108C–158C above air temperatures and reach values that would be likely to strongly

exacerbate photoinhibition. Different responses might therefore be expected when gaps form

during cloudy versus clear periods.

CONCLUDING REMARKS

The response of individual plants to spatial and temporal heterogeneity depends on the scale

of the heterogeneity. The temporal scale is paramount because it determines whether adjust-

ments in physiological properties rely primarily on relatively rapid and low-cost regulatory

mechanisms such as regulation of enzyme catalytic capacity and stomatal opening or whether

Days from start of

ap treatment

(relative)

Amax (µmol m

−2

−1

)

−50

0.4

0.6

0.8

5101520

FIGURE 7.9 Dynamics of photosynthetic acclimation and photoinhibition as indicated by reduced

ratios following transfer of Alocasia macorrhiza plants from a shade environment simulating

the understory to a gap environment in which 2 h of direct sunlight were received each day. The transfer

occurred at the arrow. The filled circles show the response of leaves that had fully developed in the shade

before the gap treatment. The open circles show the response of leaves that developed after the gap

treatment commenced. The data point connected by the dashed line shows the maximum Amax achieved

by leaves in the gap environment. Note the strong photoinhibitory decline and recovery (acclimation) in

the shade developed leaves but complete absence of photoinhibition in the gap developed leaves.

(Adapted from Mulkey, S.S. and Pearcy, R.W., Funct. Ecol., 6, 719, 1992.)

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244 Functional Plant Ecology

plasticity involving regulation of the amounts of enzymes and plant morphological changes

provide a benefit. Responses to temporal changes on a timescale of a day or less primarily

involve regulation of activities and stomatal behavior, whereas responses to longer-term changes

in the light environment involve acclimation and morphological plasticity (Figure 7.10). The

available evidence suggests that acclimation of photosynthetic capacity depends on the mean

daily integral of PFD rather than the peak PFDs. This provides a mechanism that minimizes

potentially costly responses to unpredictable variations such as sunflecks. However, the

mechanism by which plants sense the daily integral of PFD and then make adjustments

leading to the proper acclimation state is not understood.

The response to the spatial scale of heterogeneity appears to be linked principally to the

temporal scale. Sunflecks and light gradients within canopies have similar spatial scales but

since the light gradient is more predictable, acclimation is the principal mechanism for

adaptation to this heterogeneity, whereas for sunflecks regulatory mechanisms are overriding.

There is evidence that interplant communication may play an important role in acclimation to

spatial heterogeneity. The evidence is strongest for clonal plants, but patterns of branch

growth and suppression in response to spatial light heterogeneity may also involve some

branch to branch communication. The signals underlying these communications are poorly

understood but could involve hormones or resource supplies such as carbohydrates. More

research is needed to understand the nature and the role of these mechanisms in determining

how plants respond to environmental heterogeneity.

Understanding physiological responses to heterogeneity requires understanding how its

consequences scale-up. Acclimation of leaf gas exchange properties obviously influences

carbon uptake per unit leaf area, but because it also involves changes in LMA it has

consequences for carbon partitioning. Indeed, these latter effects may be more significant to

whole-plant carbon gain than the direct effects of photosynthetic acclimation. A consequence

of the scaling is that plasticity in photosynthetic properties such as Amax may lead to greater

homeostasis in growth and resource use efficiency. It is never enough to offset the wide

variation in light levels inherent in natural communities but nevertheless is important in

survival spatially and temporally heterogeneous environments.

Sunflecks

short-term, unpredictable

Gaps

long-term, predictable

Metabolite

pool changes

Light regulation

PCRC enzymes

Stomatal

regulation

Enzyme, membrane

biosynthesis, turnover

Leaf development

AcclimationRegulation

−1

01234

5 7 min h day week6 s

time

FIGURE 7.10 Ranges of time constants for various processes in relation to the timescales of sunflecks

and gap dynamics.

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Responses of Plants to Heterogeneous Light Environments 245

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