Shade plants can increase their interception of light by producing large leaves. Some of the largest leaves produced by plants are found in rainforest understoreys (Figure 12.3). Leaf size can even change within an individual plant, smaller leaves are produced near the top, where irradiance is highest, and larger leaves towards the interior and base, where light levels are lower. Another way to change light interception is by changing leaf angle and/or orientation. Vertical arrangements enhance interception of light at low sun angles during early morning or late afternoon, and reduce interception at solar noon when radiation levels are highest. Horizontal leaves will intercept light all day long, but especially around midday. Accordingly, leaves in a rainforest tend to be vertical in emergent crowns and horizontal in the understorey. Similarly, pendulant leaves of many Australian trees such as eucalypts that typically occur in high light environments represent an adaptation that helps avoid excess midday radiation.

Many plants can change their leaf angles and orientation in response to a change in light. For some, to increase interception while for others, to avoid high light. A good example of optimising light interception through leaf movement is given by Oxalis oregana, an understorey herb of redwood forests in western USA (Figure 12.4). This plant is able to track sunlight on dull days, but can change leaf angle from horizontal to vertical in only 6 min, if exposed to full sunlight. In this way, leaves can maintain maximum photosynthetic rates under a variety of light conditions but can avoid photoinhibition of photosynthesis by leaf folding. Omalanthus novo-guinensis, an Australian rainforest plant, can also change leaf angles within about 20 min in response to full sunlight (Watling et al. 1997b).

Another way of reducing light capture is a change in leaf-surface properties. Many plants in high light environments have a high reflectance of their leaves from a coat of hairs or wax or even salt crystals. Cotyledon orbiculata, a crassulacean acid metabolism (CAM) plant from southern Africa, produces a wax coating on the leaves. Plants grown at high light produce copious quantities of white wax which reflects 60% of incident light whereas plants grown in low light produce very little wax and leaf reflectance drops to 9% (Figure 12.5). Young eucalypt leaves also produce wax, while leaves of Celmisia longifolia, the snow daisy of the Australian Alps, are covered in a thick layer of silvery fibres. In these instances, plants are avoiding high light by creating their own shade, but does leaf anatomy adjust to environments where light is limiting?

Epidermal cells in some rainforest shade-adapted species are shaped to enhance light capture by acting as a lens. The optical properties of such cells focus incident sunlight into the layer of photosynthetic tissue just below the epidermis, reducing light lost due to reflectance and transmittance.

Light interception can also be regulated at a tissue and organelle level. Photosynthetic tissue can be concentrated equally on both sides of a leaf (isobilateral) to maximise light absorption from either side, or preferentially on one side (dorsiventral) as is common in species where leaves are predominantly horizontal.

Chloroplast density and location within leaves is also sensitive to the light climate, and energy capture varies accordingly. Alignment along vertical cell walls will reduce overall absorption of incident light, and in Oxalis leaves absorbance can be reduced 20% when chloroplasts align less to the horizontal and more to the vertical walls of mesophyll cells.

Once sunlight has been intercepted by an assimilatory organ, photon absorption then depends on the extent and nature of light-absorbing pigments in the photosynthetic tissues. In terrestrial plants, the major light-absorbing pigments are chlorophylls a and b plus a range of carotenoids which can act as accessory pigments. Compared with high-light plants, plants grown in low light tend to allocate relatively more resources to their light-harvesting pigments and the associated proteins than to the enzyme Rubisco and other soluble proteins involved in CO₂ fixation. This shift in allocation of nitrogen-based resources can be accompanied by marked changes in leaf anatomy, especially depth of mesophyll tissue (see Case study 12.1) and reflects a need for increased efficiency of light absorption when sunlight is limited.

There are also differences in chloroplast structure between plants grown in low light and high light. Shade chloroplasts tend to be larger than those found in sun plants. They also contain more thylakoid membranes which show higher levels of randomly arranged granal stacking into appressed regions, as shown by the extreme development of grana in Figure 12.6. The higher proportion of appressed to non-appressed membranes found in shade chloroplasts is the result of increased photosynthetic system II (PSII) and antenna (LHCII) content. LHCII is thought to be involved in thylakoid appression and formation of granal stacks. Plants grown in low light also tend to have lower Chl a/b ratios. Chlorophylls a and b are both associated with the light-harvesting antennae, while only Chl a is found in the reaction centres. A lower a/b ratio, therefore, reflects an increase in LHCII complexes relative to reaction centres (see Chapter 1, Section 1.2).

In addition to differences in leaf anatomy and chloroplast fine structure, energy derived from absorbed sunlight is processed in ways that differ subtly between shade-grown and sun-grown plants. In high light, there is a requirement for greater capacity in both the light and CO₂ fixation reactions of photosynthesis. Photosynthesis–light response curves for shade and sun plants (Figure 12.7) illustrate such differences. The initial slope of each light response curve represents the quantum or photon efficiency of photosynthesis. This is the same for sun and shade plants. The reason it does not change is that the efficiency of the light reactions is the same irrespective of how much light has been received during growth (i.e. eight photons are required for the evolution of one molecule of O₂ and fixation of one molecule of CO₂ in all plants).

However, sun plants tend to have a greater capacity for photosynthetic electron transport (greater abundance of transport components such as Cyt b₅₅₉, Cyt b₅₆₃, Cyt f and plastoquinone). They also have a greater capacity for ATP synthesis per unit of chlorophyll compared with shade plants. Taken together, these capacities of sun plants allow more sunlight to be processed into ATP and NADPH for use in CO₂ assimilation and other synthetic events. Such capacity is also matched by a greater investment in enzymes of the photosynthetic carbon reduction (PCR) cycle, resulting in a higher light-saturation point and a higher maximum rate of photosynthesis (P_max) for sun plants (Figure 12.7). As a further distinction, sun leaves tend to be thicker and have more cell layers. They also have higher stomatal conductances to facilitate rapid uptake of CO₂.

A higher photosynthetic capacity in sun plants does, however, incur some costs. The sun leaves tend to have higher respiration rates which increases the light-compensation point relative to shade plants (Figure 12.7). Higher respiration rates probably result from (1) increased carbohydrate processing in high light, (2) increased costs of constructing sun leaves and (3) a higher cost of maintaining sun leaves. Further details on maintenance costs are given in Chapter 5, Section 6.5.

Greater transpiration is a further cost of the higher photosynthetic capacity as a result of higher stomatal conductance. Sun plants often respond to the greater transpiration by increasing their root : shoot ratios. Under conditions where water is limiting, however, stomatal conductance may be reduced, sacrificing photosynthesis in favour of slower transpiration.

In the light-response curves for photosynthesis (Figure 12.7 above), photosynthesis is regarded as light limited in the initial linear region of the curve. However, at higher photon irradiances once the light-saturation point (that is, the maximum rate of photosynthesis) has been reached, further increases in light will exceed the energy-utilising capacity of that photosynthesising leaf. Refer to the dashed lines in Figure 12.7 which represent a continuation of the initial rate of photosynthesis (quantum yield of photosynthesis) and demonstrates the actual light absorption. The extent to which this absorbed light is not ‘gainfully employed’ for photosynthesis is set by P_max (the light-saturated rate of photosynthesis in normal air). At low light (< 100 µmol quanta m^–2 s^–1), both sun and shade leaves use more than 80% of the absorbed light for photosynthesis. However, once P_max has been reached, all additional absorbed light is in excess of that which can be used in photosynthesis.

Since shade plants have a lower P_max than sun plants, they experience more excess light at a given photon irradiance above saturation. Additional stresses such as drought, nutrient limitation or temperature extremes can also lead to a reduction in P_max and thus increase the probability of plants being exposed to excess light. However, even the most hardy sun plant will reach P_max at less than full sunlight (incident beam normal to leaf surface). At that level (say, 1000 µmol quanta m^–2 s^–1), approximately 25% of absorbed energy is used to drive photosynthesis, but at full sunlight (c. 2000 µmol quanta m^–2 s^–1) as little as 10% is used (Long et al. 1994). Individual leaves on plants growing in full sun commonly experience such excess light intensities. This is potentially damaging, and plants adapted to full sunlight have evolved a number of mechanisms for either avoiding excess light or for dissipating the excess absorbed energy.

Mechanisms for avoiding high light interception such as changes in leaf angle and surface features (described above), forestall absorption of excess energy. Rapid responses, such as changes in leaf angle in Oxalis and Omalanthus, occur in a matter of minutes and can regulate light interception on a diurnal basis. Slower-acting mechanisms, including production of wax on leaves, will be useful where there has been a sustained change in the light environment. These kinds of mechanisms constitute external photoprotection (Figure 12.8).

Absorption of excess sunlight as outlined above often leads to photoinhibition of photosynthesis, that is, defined here as a light-dependent decrease in the photon yield of photosynthesis (Figure 12.9). Photoinhibition is one of the most important regulatory mechanisms in photosynthesis, and results from a series of internal photoprotective mechanisms which act to reduce the amount of energy reaching the photochemical reaction centres of photosystem II (PSII). One immediate consequence of reducing light energy to PSII is a reduction in photon yield (expressed in terms of absorbed light).

Shade plants have an even greater need to dissipate excess light interception because they absorb more light (more chlorophyll per unit leaf mass), but need less light to saturate photosynthesis. Prolonged exposure of plants to excess light induces photoprotective processes that reduces the photon yield of photosynthesis, but P_max remains unchanged (curve A). However, further exposures to excess light will result in both photon yield and P_max being reduced (curve B). The photosynthetic rate is then reduced at all light levels as a consequence of the photoprotection.

Photoprotection is normally sufficient to cope with light absorbed by leaves; the more extreme photodamage only occurs when the capacity for photoprotection is exhausted. Photodamage is manifested as a decline in both photon yield and P_max, and recovers very slowly (hours to days), whereas photoinhibition and photoprotection recovers much faster (minutes to hours). Severe photodamage results in bleaching of pigments and damage to membranes (photo-oxidation) and may lead to tissue death.

Consider the alternative fates of light energy absorbed by a leaf and their relevance to photoprotection, photoinhibition and photodamage (Figure 12.10). Although blue light has higher energy and causes excitation to a higher excited state, this energy is quickly lost as heat, and chlorophyll molecules drop to a lower excited state. Utilisation of energy from excited chlorophyll molecules results in either assimilatory or non-assimilatory photochemistry, thermal dissipation or release of light of a longer wavelength (fluorescence). The proportion of absorbed energy consumed by these different processes dictates their comparative significance, and in order of importance as protective devices they are:

1. Assimilatory photochemistry, leading to fixation of CO₂ into stable chemical products;
2. Non-assimilatory photochemistry, that is, energy consumption by metabolic processes that do not result in fixation of CO₂ into stable chemical products, including photorespiration, nitrate reduction and the Mehler reaction. All consume energy but there is no net gain in carbon as a result;
3. Conversion of light energy into heat (thermal dissipation);
4. Re-emission of photons as fluorescence. Emission of in vivo Chl a fluorescence is revealed dramatically during measurements (Chapter 1, Section 1.2.5). Such emission still accounts for only 1% of energy derived from absorbed light.

Most of the NADPH and ATP formed during photosynthetic energy transduction is stored as stable photosynthetic products. Some is consumed in photorespiration and nitrate reduction. Because these non-assimilatory processes also utilise NADPH and ATP, they help reduce the need for photoprotection. The Mehler reaction, in which electrons flow to O₂ via photosynthetic system I (PSI) (Chapter 1, Figure 1.10), still supports electron flow and thus might also reduce a need for photoprotection.

However, if photochemical capacity is exceeded by incoming energy, a plant will engage photoprotective mechanisms which increase the amount of energy dissipated as heat. This non-photochemical conversion of light energy is thought to occur in the PSII antennae and involves a group of pigments known as xanthophylls and includes violaxanthin, antheraxanthin and zeaxanthin (Figure 12.11). These are a special group of carotenoid pigments which undergo interconversion in response to excess light. Energy is dissipated in the process. In low light, violaxanthin predominates, but when light is in excess, conversion to zeaxanthin via antheraxanthin occurs. This conversion requires a low pH, ascorbate and NADPH. Such conditions exist in the lumen of chloroplasts in high light. Zeaxanthin, and possibly antheraxanthin, provide photoprotective thermal dissipation of the excess light energy. When light levels are no longer excessive, zeaxanthin slowly converts back to violaxanthin via antheraxanthin (Figure 12.11). Total pool sizes of the xanthophyll pigments increase with increasing exposure to excess light. Sun plants can have three- to four-fold larger pools of violaxanthin, antheraxanthin and zeaxanthin than shade plants and the presence of other stresses can also result in increases in pool size.

Internal differences between sun and shade leaves with respect to energy dissipation are also apparent in the different patterns of attenuation of light through mesophyll tissues, such as in succulent CAM plants such as Cotyledon orbiculata. There, xanthophylls are mostly found in outermost cell layers where the light environment is strongest. If the reflective wax coating is intact, no internal photoprotection is required at the growth irradiance and there is no zeaxanthin formed. However, if the surface wax (external photo-protection) is removed by hand, internal photoprotection is then needed and zeaxanthin appears in the outermost layer (Figure 12.12).

Overall activity of the xanthophyll cycle varies with mesophyll irradiance, while the concentration of particular components also varies according to tissue depth. Changes in concentration of the various components of the xanthophyll cycle are shown here for successive (1 mm) layers in thick leaves of C. orbiculata, with and without their wax coating. In waxed leaves at the end of a dark period (top figure, Figure 12.12) xanthophyll cycle pigments are represented mainly by violaxanthin (V) with a small amount of antheraxanthin (A). After 6 h exposure to high light (middle figure, Figure 12.12) a small amount of violaxanthin is converted to antheraxanthin, but no zeaxanthin (Z) is formed, indicating that the natural wax coating on these leaves is protecting chloroplasts from excess light. Physical removal of surface wax (brushed leaves in bottom figure, Figure 12.12) results in zeaxanthin production within the uppermost layer of leaf tissue but not in deeper tissues or lower surfaces. Restriction of this xanthophyll cycle component to the top section confirms that zeaxanthin accumulation is a response to excess light.

A seed germinating in a rainforest understorey starts life in a low light environment. This will not present major problems to an obligate shade species which cannot tolerate strong sunlight; such species have adapted to life in an understorey. However, many rainforest species are better described as either shade tolerant (i.e. able to germinate and persist in low light, but requiring higher light to reach maturity) or shade intolerant (unable to germinate or grow in low light). In successional terms, shade tolerance is a feature associated with climax species and shade intolerance with pioneer species.

Shade-tolerant species can persist as seedlings in the understorey, often for years, while still being able to respond to an increase in light availability when it occurs.

By comparison, shade-intolerant (early-successional) species can only germinate and grow where there is ample sunlight, and consequently they tend to occur in wide gaps and on forest edges. Wide gaps are relatively rare in old-growth rainforests which have been undisturbed by logging or slash and burn agriculture. Shade-intolerant species are unable to maintain a positive carbon balance when growing in low light. The change from a high light to a low light environment requires a change in allocation of plant resources as described in the quantitative growth chapter (Section 6.2). Shade-intolerant plants are unable to make this change and are burdened with the higher costs of construction and maintenance of leaves better suited to strong sunlight

Germination

Shade-intolerant species tend to produce numerous small seeds throughout the year which are widely dispersed. Their seeds are also able to remain viable for long periods (years) by going through a period of dormancy. This is often broken by high temperature or strong direct sunlight with a high ratio of red to far-red irradiance (R:FR ratio decreases with sunlight attenuation through canopies). Such environmental cues for germination are all experienced in wide gaps. Following germination, seedlings show rapid growth to maturity, allowing them to become well established in a gap before other slower growing species. These characteristics increase the probability of success for shade-intolerant species in the heterogeneous light environment of a rainforest.

Shade-tolerant species, on the other hand, have evolved a different suite of characteristics. They tend to produce a few large seeds which are generally not well dispersed, with little or no dormancy. However, the seeds have the ability to germinate in low light and persist in the understorey as seedlings for years. A rarity of gaps and a lack of dormancy found in most shade-tolerant species increases the probability of establishing in a low-light understorey environment. In situations like this, the larger seed provides seedlings with a reserve which they can draw upon during early establishment. In rainforests, tree seedlings survival in understorey habitats is positively correlated with seed size, especially in the first few months following germination.

Following establishment in the understorey, seedlings of shade-tolerant species may have to wait a long time before a gap appears overhead. Many species succumb to attack from herbivores or pathogens or may be crushed by large animals (including humans!). Those that do survive must be able to acclimate to the new conditions arising on gap formation; their ability to do this will depend on the nature of the new microclimate and the acclimation potential of each species.

Growth response to high light

Emergent trees of tropical rainforests have to endure strong sunlight, and leaves comprising the crowns of such trees will have acclimated to full sun. In young-growth forests, canopy emergents are early-successional fast-growing species that are adapted for fast growth in full sun on large disturbances. Such species represent an initial phase in forest dynamics that might last 10–20 years. By contrast, in old-growth forests, early-successional species have long since completed their life cycles, and will have been replaced by later-successional species whose seedlings initially tolerated deep shade on the forest floor, but now endure full sun as canopy emergents. Such remarkable plasticity is an adaptive feature of late-successional species and involves sun/shade acclimation by individual leaves.

The differences in growth rate of early-successional fast-growing species versus later-successional and shade-adapted species is illustrated in Figure 12.13 by two rainforest species that are important in the timber industry: the sun-loving red cedar (Toona australis) and the shade-adapted tulip oak (Argyrodendron sp.).

A detailed study of three rainforest species from North Queensland was conducted by Thompson et al. (1992a, b). The red cedar Toona australis (an early-successional species) and two species of tulip oak Argyrodendron (late-successional species) showed different acclimation potentials when grown under a range of light conditions (Figure 12.14).

When grown under high light, 535 µmol quanta m^-2 s^-1,which is typical of average canopy radiation in a tropical rainforest, T. australis achieved a higher P_max and light-saturation point than either of the Argyrodendron species. However, T. australis was more sensitive to nutrient levels, being unable to acclimate to the same degree in low-nutrient compared to high-nutrient regimes. Moreover, fast growth in T. australis was greatly promoted by a positive light x nutrient interaction on leaf expansion and photosynthetic capacity; adaptive features with a clear selective advantage on open sites where soil disturbance liberates nutrients.

Toona (sun loving) produced a much greater depth of mesophyll tissue under strong light compared to weak light (Figure 12.15b), which accounted for enhanced photosynthetic capacity. Argyrodendron sp. (shade adapted) was much less responsive to photo irradiance during growth, producing consistently thicker leaves regardless of light level, but with lower photosynthetic capacity.

These adaptations result in the more vigorous growth of Toona than Argyrodendron at high light.

Formation of gaps provides an important opportunity for many rainforest plants to escape from the dim understorey environment and reach maturity as canopy trees. Rainforest habitats actually present a continuum of light availability ranging from almost total shade (diffuse light) through intermediate levels of direct and diffuse sunlight to a wide gap where direct sunlight is received for most of a day. Input of direct sunlight beneath a closed canopy can be surprisingly high because of sun patches and more transient sunflecks. Sun patches occur when small and variable openings in the overlying canopy permit direct sunlight to penetrate to the forest floor, resulting in the familiar patchwork of sunlight and shade which can be seen in any understorey on a clear day (Figure 12.16).

Competition for light is intense, and a sunfleck shown passing over this tiny population would be providing a much-needed source of sunlight, namely a few minutes of around 1,500 µmol quanta m^-2 s^-1 compared with background photon irradiance of around 150 µmol quanta m^-2 s^-1.

Patches of sunlight move across the forest floor on bright days, and will illuminate any leaves or parts of leaves which lie in their path (Figure 12.17). Daily total photon irradiance on the occasion of the measurement shown in Figure 12.17 was 6.0 mol quanta m^-2 d^-1). The abrupt increase from a background level of around 50 µmol quanta m^-2 s^-1 to 1,750 µmol quanta m^-2 s^-1 energises photosynthesis, but is counteracted by increased leaf temperature, especially during prolonged exposures. Transpiration cooling is a significant component of heat budgets for such large leaves, so that adequate soil moisture is a prerequisite for continuing leaf gas exchange during a sunfleck.

Sunfleck frequency will be an additional factor for carbon gain during exposure to strong photon irradiance. Photosynthetic induction state diminishes to a minimum after 30 min in low light (see Figure 12.18 below) and some minutes are required to regain full capacity in strong light. Infrequent sunflecks are thus used with reduced efficiency.

Sunflecks and sun patches are of potential use to understorey plants for photosynthesis, but is this potential realised? Growth of understorey tree seedlings has been shown to be correlated with the amount of direct light received in sunflecks, and up to 60% of carbon gain in such environments has been attributed to this source. However, when compared with expected values based on the known steady-state response of plants to light, sunfleck utilisation is often below predicted values (Pfitsch and Pearcy 1989). Moreover, species vary in their capacity to utilise sunflecks. Watling et al. (1997a) measured the growth of four Australian rainforest species under simulated sunfleck regimes and showed that sunflecks contributed to growth in two species (Diploglottis diphyllostegia and Micromelum minutum), whereas the other two species (Alocasia macrorrhiza and Omalanthus novo-guinensis) were unable to make effective use of sunflecks.

Factors underlying this variation in sunfleck utilisation efficiency

Two components of a plant’s photosynthetic physiology will determine how the light in a sunfleck is used. Firstly, photosynthetic capacity (P_max) will set a ceiling on the amount of light a plant can use. Secondly, a few minutes of illumination at least are needed for PCR cycle intermediates to reach critical levels, and this ‘induction requirement’ of photosynthesis determines how quickly a leaf can respond to an increase in photon irradiance.

Measured photosynthetic capacities of understorey plants are often low. When a leaf experiences a sunfleck, carbon fixation will increase to the point of light saturation. If an understorey plant could increase P_max, it could utilise more light. But there are trade-offs. For example, higher respiration rates would increase the light-compensation point, and increase carbon losses during the low light periods separating sunflecks.

Regardless of photosynthetic capacity, the ability of a plant to use sunflecks is also affected by the induction requirement of photosynthesis. When a leaf that has been in low light for some time is exposed to an increase in photon irradiance, the rate of photosynthesis does not increase instantaneously to the new level. Instead, there is a gradual increase in assimilation which can take from 10–60 min for completion. This ‘induction period’ varies according to species as well as the induction state of the leaf concerned. Three different processes are involved; namely (1) buildup of PCR cycle intermediates and in particular ribulose-1,5-bisphosphate (RuBP), (2) light-dependent activation of Rubisco, and (3) light-dependent opening of stomata. Each of these processes follows a different time-course. Buildup of a metabolite pool is fastest (1–2 min), followed by Rubisco activation (2–5min) and finally stomatal opening (up to 60 min). Relaxation in low light is more protracted but generally occurs in the same sequence, leading to a decline in the induction state.

Thus, the longer a leaf has been in low light, the lower it’s the induction state. Figure 12.18 illustrates this for a leaf of Alocasia macrorrhiza, a plant common in rainforest understoreys and forest edges in eastern Australia. Fully-induced leaves were transferred to low light (10 µmol quanta m^-2 s^-1) for different lengths of time (up to 60 min). Their induction state was determined as the proportion of light-saturated photosynthetic capacity (P_max) achieved within 2 min after return to saturating light. Induction loss in Alocasia, therefore, has a half time of about 25 min, but other species have been found to be either faster (e.g. Adenocaulon bicolor, an understorey herb from the redwood forests of western USA; Pfitsch and Pearcy 1989) or slower (e.g. Castanospora alphandii, a shade-tolerant tree from Australian rainforests; Watling et al. 1997a, b).

Chazdon and Pearcy (1986) showed that continuous light is not needed for induction to proceed. If leaves were subjected to a series of 60 s lightflecks (artificial sunflecks) separated by 2 min of low light, then induction state increased with each successive lightfleck. In nature, sunflecks are often clustered with a sequence of irregular bursts, separated by dull periods of variable duration. Under these circumstances, the state of induction might improve such that a plant will respond more rapidly to closing sunflecks in each sequence. This is supported by the data of Chazdon and Pearcy (1986), where the efficiency with which a sequence of lightflecks was utilised increased with successive lightflecks (efficiency was calculated as the actual amount of carbon fixed during a lightfleck relative to the amount predicted if there had been no induction period).

Carbon gain by fully induced leaves during lightflecks can exceed that expected, resulting in improved efficiency of light utilisation. This ‘intermittency phenomenon’ was noted by Kriedemann et al. (1973) in grapevine leaves exposed to high-frequency lightflecks. Similar investigations in a number of other species have also shown that such enhancement occurs only with short-duration lightflecks and is more prominent in fully induced leaves. Alocasia macrorrhiza showed improved efficiency of lightfleck utilisation by fully induced leaves only when lightflecks were of 40 s duration or less. Un-induced leaves needed lightflecks 10s or shorter (Chazdon and Pearcy 1986).

This apparent improvement in light use efficiency results from continued carbon fixation in low light (or darkness) following a lightfleck. During a short lightfleck, pools of triose phosphate and RuBP build up because carbon fixation runs transiently slower than the light reactions. This pool of PCR intermediates is then used for post-illumination CO₂ fixation. In rainforest understoreys, where sunflecks are generally longer than a few seconds, this kind of enhancement is unlikely to be important. However, it may contribute significantly to carbon gain under crop canopies, where sunflecks are much shorter and more frequent.

One consequence of generally low photosynthetic capacities in understorey plants is a limited ability to process the light energy they absorb during strong sunflecks. This limited ability can also be exacerbated by a low induction state. Under these conditions, understorey plants will need to dissipate excess energy if they are to avoid photodamage. Field measurements of chlorophyll fluorescence from A. macrorrhiza show a decline in the quantum yield of photosynthesis (measured as F_v/F_m) during saturating sunflecks, indicating that photoprotective mechanisms are probably being engaged. Simultaneous assessment of the xanthophyll pigments shows that interconversion of violaxanthin to zeaxanthin is also occurring. After the sunfleck has passed, conversion of zeaxanthin to violaxanthin is extremely slow in species such as A. macrorrhiza, perhaps allowing a more rapid photoprotective response for subsequent sunflecks. However, quantum yield increases more rapidly than xanthophyll reconversion on return to low light, demonstrating a requirement for both high ΔpH and zeaxanthin for internal photoprotection to occur (Watling et al. 1997b).

Engagement of photoprotective mechanisms by shade-tolerant plants in an understorey environment may seem surprising, but serves to illustrate the extent of spatial heterogeneity in resource availability which is a feature of most habitats.

Interception of light by a crop canopy is strongly related to total or canopy leaf area. A crop will thus intercept more light and hence grow faster if it develops the canopy leaf area rapidly. This principle applies to both annual crops, which are usually planted at the beginning of a growing season and to perennial crops, which resume growth after a dormant season. Leaf area development of sugar cane, for example, is generally slower in the year of planting compared with a subsequent ratooned crop, where canopy regrowth is enhanced by stored photoassimilates. By analogy with early canopy expansion, retention of green leaves late in a growing season also extends light interception and enhances storage of photoassimilates. This is also true for perennial crops. For some deciduous horticultural crops, leaf area expansion is also rapid because of preformed primordia which emerge rapidly and comprise the largest leaves (Greer 1996).

The leaf area index (LAI) is the ratio of total projected leaf area (one side only) per unit ground area, and is widely used to characterise the canopy light climate. A canopy where LAI equals 1 has a leaf area equal to the soil surface area on which it grows. This does not mean all light is intercepted, because some leaves overlap, leaving gaps. Moreover, not all leaves are positioned at right angles to the incident radiation. A crop under favourable growing conditions increases LAI rapidly during early development to a maximum of 3 to 7.

An example of LAI development of three tropical cereal crops grown under well-watered conditions in South East Queensland is given in Figure 12.19. Sorghum showed a more rapid increase in LAI than did maize, largely because of a higher sowing density (33 v. 5.6 plants m^–2). A late maturing rice crop showed slowest leaf area development during early stages of growth, but the maximum LAI was none the less higher for rice than for maize. As a general rule, maximum LAI is achieved just prior to flowering in cereal crops. By that stage, growing points are differentiating floral rather than leaf primordia, and initiation of new leaves has ceased.

Some cereal crops lose leaves and the LAI declines during grain filling as crops mature. Differences in LAI development among the three crops (Figure 12.20a) are evident in light interception by the respective canopies (Figure 12.19b); interception prior to 60 d was highest in sorghum and lowest in rice. However, in all three crops, canopy light interception increased rapidly during early stages of growth. Incident radiation was almost completely intercepted once a high LAI had been achieved.

Despite wide variation in crop phenology, sunlight interception and LAI maintain a tight curvilinear relationship (Figure 12.19c). Thus, interception increases sharply with increases in LAI to about 90% once LAI exceeds 4, and approaches an asymptote at higher LAI, see also Figure 12.20 from Khurana and McLaren (1982). In this research on potato, numerous treatments were imposed, involving different storage of seeds at low temperatures including apically and multisprouted seed treated at 4 and 12 °C and then at 8 °C before planting. In Treatment1, the trial included unsprouted seed stored at 4 °C, in Treatment 2, the trial included seed stored in the dark and in Treatment 3, two additional sprouting treatments were mixed alternately along the row. Such a relationship between LAI and light interception applies to many crops, and emphasises (1) the importance of a rapid increase in LAI during early stages of growth, and (2) a requirement for only moderate LAI to achieve effective light interception. Indeed, excessive leaf area development can be counter-productive, because reproductive development, and hence economic yield, may be reduced due to self-shading and resource allocation to leaf production (such as for fruit trees and grapevines, Section 12.4).

The time-course of light interception during crop growth can be manipulated to some extent by farmers. For example, seeding rate is an important management option which affects interception and subsequent crop growth and yield. A high seeding rate would produce a high plant population density and a high LAI at crop establishment. This hastens canopy interception and hence biomass production would be promoted. Any advantage of a high plant density may, however, disappear with time during crop growth, because radiation interception of a medium plant density may eventually catch up with that of the high density (Figure 12.21).

In this case, density 3 (35 plants m^–2) was sufficient for radiation interception and plant dry matter production. If plant density is very low, shown as density 1 (1.4 plants m^–2) or density 2 (7 plants m^–2) in Figure 12.21, LAI never exceeded 2 and final biomass at harvest was much smaller than values returned from higher densities. Solar radiation was not fully intercepted and hence wasted at low planting density, and potential yield (dry mass produced per unit area) was never realised.

As solar radiation penetrates a crop canopy, PAR is intercepted by leaves and photon irradiance commonly declines exponentially with cumulative leaf area (i.e. depth in Figure 12.23), according to the exponential relationship:

\[ I = I_0 e^{-kL} \tag{12.1} \]

where \(I\) is horizontal photon irradiance within a canopy, \(I_0\) is horizontal photon irradiance above that canopy, \(L\) is LAI from the top of the canopy to the point where \(I\) is determined, and \(k\) is an extinction coefficient (a more explicit formulation for PAR attenuation through a forest canopy is given in the next section).

Large \(k\) values imply that photon irradiance decreases rapidly with depth, whereas a canopy with a small \(k\) would allow solar radiation to penetrate deeply, for a similar leaf area profile. Variation in \(k\) value is commonly associated with leaf angle. Canopies with more horizontal leaves, such as sun-flower or cotton, have large \(k\) values, often 0.7–1.0, whereas those with more erect leaves, such as barley and sugar cane, have small values, often 0.3–0.6.

Irrespective of the canopy extinction, there is a strong relationship between the light intercepted by the canopy over the growing season and the total dry matter produced for a number of crops (Fig. 12. 22). Thus, it is imperative on growing crops to manage the LAI to achieve maximum light interception from the early part of the season to maximise production of dry matter.

 

Sunlight intercepted is not utilised with similar efficiency by different crops. There are clear differences in light use efficiency between crop species, particularly between those with C₃ and those with C₄ photosynthetic pathways. The photosynthetic advantage of C₄ species at a leaf level is evident here at a canopy level, where efficiency is higher by 30–100%. Expressed in terms of dry mass formed (g) per unit of photosynthetically active energy absorbed (MJ), the efficiency of sorghum and maize (C₄ photosynthesis) in Figure 12.19 was 1.32 g MJ^–1, while that of rice (C₃ photosynthesis) was only 0.93 g MJ^–1.

Canopy structure, and particularly the spatial distribution of leaf angles, has an important bearing on the canopy light climate and energy conversion. Large leaf angles, with leaves close to vertical, ensure good light penetration when solar angle is high, and a high proportion of leaves receive similar photon irradiances. An even distribution of light at leaf surfaces is advantageous for canopy photosynthesis and improves light use efficiency over canopies where upper horizontal leaves intercept most solar radiation and lower leaves experience greatly attenuated levels. Small and erect leaves, particularly in top canopy layers, are thus a key feature of an ideal plant type, or ‘ideotype’ for high-density cropping (Figure 12.23).

Canopy radiation climate is especially complex in mixed crops and pastures where species with contrasting forms grow together. In grass–legume pastures, grass is generally taller than the legume component and is better placed to intercept incident radiation. Legumes then exist in permanent shade. Height is, therefore, an important determinant of light interception within a mixed sward, and thus species composition. In such mixed swards, management options such as nitrogen fertiliser application, grazing time or cutting frequency all affect the relative height and hence radiation interception by component species. High-nitrogen fertiliser tends to favour grass, while clover may become dominant under nitrogen-limiting conditions.

Light profiles within a pasture are, therefore, affected by LAI profiles of component species (Figure 12.24), and a clover-rich sward with more horizontal leaves (N₀, no added nitrogen) shows stronger attenuation of sunlight than a grass-rich sward with a preponderance of vertical leaves (N₂₂₅, nitrogen added). In common with monocultures, pasture productivity is enhanced by a species balance that ensures even distribution of sunlight within a mixed community.

In a complex system like a rainforest, the canopy is arranged in horizontal layers, the distribution of leaf area with height being associated with the development in space and time of the diversity of species. However, even in monocultures it is convenient to consider the canopy as being horizontally uniform and the level of radiation constant in any layer. Even here, attenuation of light through the canopy is complicated by changing availability, quality and direction of incident light and it is necessary to make some simplifying assumptions when calculating the proportion of light that is intercepted.

The Beer–Lambert Law, which describes absorption of light by plant pigments in solution, provides a simple approach which has been applied widely to a range of canopies. This function demonstrates that the absorption of light will be more or less decline exponentially with increasing intercepting area down through the canopy. Absorption of sunlight by photosynthesis occurs within a well-defined spectral band (400–700 nm) and matches a peak in energy distribution across the wavelength spectrum of sunlight transmitted to the earth’s surface through our atmospheric window (as shown in Figure 12.1 at the start of the chapter).

Sunlight in this waveband can be represented as either a quantum flux or a radiant energy flux. Quantum flux, or more explicitly, photosynthetic photon flux density (PPFD, PAR), is simplified here to ‘photon irradiance’ (\(Q\)) and has units of µmol quanta m^–2 s^–1 (‘µmol quanta’ rather than ‘µmol photons’ because quantum energy derived from photons drives photosynthesis). For the sake of making a clear distinction, radiant energy flux is simplified to ‘irradiance’. In the present example, irradiance coincides with photosynthetically active radiation (PAR) and is expressed as joules (J) per square metre per unit time. Depending on the application, time can span seconds, days or years, and is then coupled with either joules, megajoules (MJ) or gigajoules (GJ).

On clear days, PAR represents about half of the total shortwave (solar) radiation or radiant energy flux \(I\) (expressed as J m^–2 s^–1) incident on a canopy, and is totally responsible for photosynthesis. If changes in the spectral distribution of energy as it passes through the canopy are ignored, \(I\) and PPFD can be used interchangeably in the analysis below. In practice, PPFD is attenuated more rapidly than \(I\) (that is, there is a proportionally larger change in PAR than total solar radiation (\(I\)) in moving from top to bottom of the canopy) because leaves are relatively transparent to the near-infrared part of the solar beam.

Application of the Beer–Lambert Law shows that at any level of cumulative area \(F\) within the canopy, the rate of change of photon irradiance, \(Q\), within the canopy is given by:

\[ \mathrm{d} Q / \mathrm{d} F = -kQ_F \tag{12.2} \]

where \(k\) is the extinction or foliar absorption coefficient, a dimensionless parameter. \(k\) measures the fraction of incident photons absorbed by a unit of leaf area or conversely the fraction of leaf area projected onto the horizontal from the direction of the incident beam. For many species, foliage in the vertical plane is distributed approximately symmetrically about the midpoint of the canopy and most absorption of light will occur in the middle of the canopy. After integration, \(Q_F\) at any level \(F\) is given by:

\[ Q_F = Q_0 e^{–kF} \tag{12.3} \]

where \(Q_0\) is the PAR incident at the top of the canopy. At the base of the canopy, \(F\) is equal to the leaf area index (LAI), a dimensionless number which expresses total projected leaf area of the canopy as a ratio of the ground area over which it is displayed. Thus the level of interceptance is an exponential function of the product \(kF\). If a value of 0.5 is assigned to \(k\), then 95% light interception occurs at \(kF = 3\) which is equivalent to an LAI of 6 m² leaf area m^–2 ground area. Maximum values of LAI vary with species, site, stress and season.

In practice, \(k\) is not a constant value for any canopy and varies with solar elevation, the ratio of direct to diffuse beam irradiance and any changes in canopy structure or leaf inclination and orientation which occur seasonally or in response to the movement of leaves (e.g. heliotropism). For the majority of canopies, \(k\) varies from 0.3 to 1.3. Canopies with erectophile leaves (e.g. grasses) and high leaf angles to the horizontal or with a clumped distribution have a lower \(k\) and intercept less light per unit of foliage compared to canopies with planophile leaves with a higher \(k\) (e.g. clovers) and low leaf angles or a regular distribution. The cumulative leaf area required to intercept 95% of the radiation incident at the top of the canopy will be greater for canopies dominated by erectophile leaves or having a clumped distribution.

In many species and plant communities, leaf inclination may change from erectophile at the top of the canopy to planophile at the bottom. This allows more even distribution and interception of light and reduces the proportion of leaves which is exposed at the top of a canopy to levels of light which are saturating for photosynthesis and, conversely, reduces the proportion of leaves at the bottom of a canopy which is exposed to levels below the light-compensation point for photosynthesis. For a canopy with leaves distributed randomly with respect to orientation and inclination, \(k\) is approximately 0.5 (Monteith and Unsworth 1990) and this value is commonly assigned to \(k\) in the literature.

Photosynthesis is driven by the fraction of radiation intercepted by the canopy and gross photosynthetic production (\(A_g\)), a measure of the total amount of CO₂ fixed in photosynthesis, can be expressed as:

\[ A_g = A_0 [1 - exp(-kS_{a}W_{l})] \tag{12.4} \]

\(A_0\) is the gross photosynthetic production at full light interception and \(S_{a}W_{l}\) expresses LAI as the product of specific leaf area (\(S_{a}\), the ratio of leaf area:leaf dry mass) and dry mass of leaf organic matter (\(W_{l}\), often approximated as leaf dry mass).

Efficiency of light conversion to biomass (\( \varepsilon \))

As implied by Equation 12.4, there is a proportional relationship between production of dry mass and interception of radiation (see Fig. 12.22), while LAI is a major determinant of photosynthetic production. The slope of this relationship is a measure of the conversion efficiency (\( \varepsilon \)) of light (photon irradiance if based on PAR) or irradiance (\(I\) if based on shortwave radiation) to dry mass. \( \varepsilon \) has units of g MJ^–1 and values based on photon irradiance are approximately twice those based on \(I\). \( \epsilon \) can be considered to be the canopy-scale equivalent of \( \varphi \), the quantum yield of individual leaves. Values of \( \varepsilon \) based on absorbed radiation are net of any light or radiation that is reflected upward from the direction in which the incident value is measured.

This proportional relationship was first clearly defined in the above terms for the seasonal growth of temperate agricultural and horticultural crops in Britain (Monteith 1977, Fig. 12.22). It has since been shown to hold for a range of vegetation types and environments. Proportionality occurs because photosynthesis by most leaves in a canopy tends to be light limited. Consequently any increase in light intercepted or absorbed results in an increase in dry mass production. As crops grow from establishment or plant communities develop from a state of initial colonisation to maturity, LAI increases, and a greater leaf surface results in greater levels of light interception and rates of growth.

As predicted by theory, linear relationships between above-ground dry mass production and intercepted radiation have been observed for eucalypts in plantation forests in southeast Australia: \( \varepsilon \) was around 0.45 g MJ^–1 (based on \(I\), Figure 12.26). Conversion efficiency was independent of species and provenance within species, and for one species, Eucalyptus globulus, was independent of site. Differences in growth rate between species, in this case during the early phase of forest growth, can be entirely a function of more rapid development of LAI in one species compared to another.

Comparative analyses of \( \varepsilon \) for different vegetation types are commonly based on above-ground dry mass (\(W_{a}\)) because of lack of information on below-ground biomass (\(W_{b}\)). \( \varepsilon \) based on \(W_{a}\) will be less than that based on \( W_{a} + W_{b} \) by the ratio \(W_{a} : (W_{a} + W_{b}) \). Partitioning of dry mass to roots may be substantially higher on a resource-poor compared to a resource-rich site. Consequently, a comparison of \( \varepsilon \) between sites based on \(W_{a}\) rather than \( W_{a} + W_{b} \) would lead to a relative underestimate of the efficiency of conversion of light to dry mass on poorer sites. Similarly, stress in response to soil water deficit, high vapour pressure deficit (leading to stomatal closure) or extremes of temperature will reduce \( \varepsilon \) and may also change the partitioning of dry mass. Reductions in \( \varepsilon \) occur in response to stomatal closure or to stresses of sufficient severity to reduce the quantum yield of photosynthesis. In effect, plants reduce photosynthesis by redirecting absorbed energy away from photochemistry and into photoprotective pathways which disperse absorbed energy as heat. \( \varepsilon \) thus embodies the photosynthetic history of a crop over a given interval and integrates the effects of all environmental variables on photosynthetic utilisation of absorbed radiation.

In summary, forest canopies consist of multiple layers. A logarithmic gradient of sunlight availability exists from upper to lower layers, and leaf properties adjust accordingly.

An upper limit on dry matter production by crops is set by the amount of visible radiation (400–700 nm) intercepted (Monteith 1977). Horticultural crops, however, rarely achieve 100% interception of sunlight because physical access is required year round for routine management operations such as spraying, pruning and picking. This is especially so for perennial fruit crops and vines, but is also the case for many annual greenhouse and vegetable crops that are repeatedly hand harvested. With a closed agronomic canopy such as a field of wheat, light interception is largely determined by LAI. With discontinuous canopies such as an apple orchard or a vineyard, a fixed LAI can intercept different amounts of light depending upon the display in space of the discrete canopy units, namely individual trees or vines. (LAI for discontinuous canopies is calculated from the total area of leaves on the plant divided by the area allocated to the plant.)

Light interception of horticultural crops can be altered by changing spacing, tree height, tree shape and/or row orientation. An illustration of this is given in Table 12.1 using a simulation model of light interception (Palmer 1989). The model calculated light interception over a whole day and allowed for change in incident radiation, sun angle (both elevation and azimuth) and sky light. The model was used to calculate light interception under sunny conditions by apple trees arranged in continuous rows, of truncated conical cross-section, in midsummer at Riwaka, Nelson, New Zealand. For a constant LAI, light interception increased by increasing hedge height, closer row spacings and planting in a north–south rather than an east–west orientation (Table 12.1). Light interception varied by a factor of two, from 27% by short wide-spaced hedges in east–west (EW) rows to 55% by tall close spacings in north–south (NS) rows. Differences due to row orientation will be smaller in cloudy regions where more of the incoming light is diffuse.

In Table 12.1, the density of leaves within the tree volume changes with height and row spacing to maintain a constant LAI. Differences in light interception would be much larger if leaf area density rather than LAI was maintained at a constant. Nevertheless, data given in Table 12.1 for discontinuous canopies show that the relationship between LAI and light interception depends on the physical arrangement of foliage in space. Calculations for Table 12.1 assume an extinction coefficient appropriate for apples. Light interception would have to be recalculated for other crops such as peach and cherry that have lower extinction coefficients (Flore 1994).

As discussed in Section 12.3, the relationship between light interception (\(F\)) and LAI of a continuous canopy follows the Beer–Lambert Law, and can be approximated by Equation 12.5. Again, \(k\) (the extinction coefficient) is dependent upon leaf angle distribution, leaf transmission to sunlight and whether the foliage is random, regular or clumped. \(k\) varies between about 0.3 for erect foliage and 1.0 for canopies comprising horizontally disposed leaves. In general terms,

\[ F = 1 - e^{–k\mathrm{LAI}} \tag{12.5} \]

Unlike closed canopy forests or a continuous crop cover, sunlight interception by discontinuous canopies consists of two parts, a fraction determined by the overall form and extent of the canopy (\(F_\mathrm{max}\)) and a leaf area part that determines how close a particular orchard approaches the maximum interception attainable. \(F_\mathrm{max}\) would be reached if LAI was infinite. Accordingly, Equation 12.5 can be rewritten for discontinuous canopies as Equation 12.6, where \(L' = \mathrm{LAI}/F_\mathrm{max}\) (Jackson and Palmer 1979).

\[ F = F_\mathrm{max} (1 - e^{–kL'}) \tag{12.6} \]

This relationship for a discontinuous canopy contrasts with that for the continuous canopy (Equation 12.5) where an infinite LAI would cause complete exclusion of light. When light interception by two of the orchards in Table 12.1 is plotted as a function of LAI (Figure 12.29) and compared with a continuous canopy with the same extinction coefficient, light interception by either orchard approached an asymptote well short of infinite LAI.

Orchards were either a continuous canopy (\(F_\mathrm{max}\) = 100%), hedgerows 2 m tall, with 3 m row spacing, 1.5 m thick at the base and 0.5 m at the top (\(F_\mathrm{max}\) = 74%) or hedgerows 1 m tall, with 5 m row spacing, 1.5 m thick at the base and 0.5 m at the top (\(F_\mathrm{max}\) = 39%). Note that light interception depended on both LAI and \(F_\mathrm{max}\), so that the same light interception can be achieved with a very different LAI or the same LAI can be rearranged to intercept a different amount of sunlight.

Light interception by discontinuous orchard canopies can, therefore, be increased by increasing LAI, but a far more effective strategy is to increase canopy extent. Put another way, it is better to use orchard design to increase \(F_\mathrm{max}\) and thereby intercept sunlight that would otherwise fall into clear alleyways, rather than intercept sunlight that had a good chance of being absorbed by other foliage. Knowing the physical dimensions of the canopy, \(F_\mathrm{max}\) can be calculated from a mathematical model. \(F_\mathrm{max}\) complex shapes can be determined from CAD graphics.

As for annual crops and forest canopies, there is also a linear relationship between biomass production and canopy light interception for horticultural crops, even though the horticultural yield is measured as fruit weight rather than biomass (Figure 12.30. Thus in all managed cropping systems, a universal relationship between canopy light interception and yield or biomass production and the LAI, whether based on continuous or discontinuous canopies, underpins this relationship through determining the extent of light interception by the canopy.

Although the upper limit of orchard dry matter production is set by light interception as outlined above, crop composition is determined by sunlight distribution within the canopy, and shade can reduce fruit quality. This is a general phenomenon among perennial fruit crops and has been reported for apple, citrus, peach, cherry, kiwifruit and raspberry. In apple, for example, fruit from more shaded regions are smaller, and have less red colour and lower soluble solids. There are also effects on apple quality after storage, with shaded fruit of Cox’s Orange Pippin tending to suffer more from shrivel and core flush and less from bitter pit than fruit from well-exposed regions of the tree. Fruit of satsuma mandarins grown in shaded regions of the trees are smaller, with a higher acid content and lower sugar content than fruit grown in well-exposed parts of the canopy.

With both peaches and cherries, shading has been found to reduce fruit colour, soluble solids and fruit size and delay abscission and maturity. Kiwifruit from shaded regions of the canopy, or individual fruit which has been artificially shaded during the season, show reduced fruit fresh weight, soluble solids, firmness and chlorophyll concentration in the mesocarp compared to well-exposed fruit. With grapevines, too, shaded fruit have generally lower sugar, total phenol and anthocyanin but higher pH, malate, potassium and titratable acidity than fruit grown in well-exposed positions in the canopy. These differences in grape quality have carried through to the wine quality made from the grapes. A consequence of decreased sugar levels in shaded grapes is a delay in harvesting. This may put crops at risk in climatically marginal regions.

Generalisations on sunlight and fruit quality have been derived from shading experiments on whole trees or parts of trees, or from correlation studies of fruit quality and irradiance in different parts of the canopy. Consequently both fruit and foliage have been subjected to reduced light, but some features in grapes and apples, such as anthocyanin development, vary according to illumination of the fruit itself. With grapes, cluster shading reduces fruit anthocyanin and total soluble phenolics, while leaf shading results in smaller berries with lower glucose and fructose content.

Shade within orchard trees can arise from self-shading or from adjacent trees or shelterbelts. Light levels in midsummer within well-spaced, traditionally pruned large peach trees can drop to 4–15% of incoming radiation. Sour cherry trees tend to be more dense, and light levels as low as 2–4% have been reported. Vigorous grape canopies can be very dense, with irradiance within the canopy reduced to less than 1% of ambient. With such dense canopies, between-row shading will be unacceptable if the ratio between canopy height and clear alleyway spacing exceeds 1:1 (Smart 1989). With the much more open canopies of apples, such ratios may be less useful, as acceptable light distribution within the trees can be obtained over a wide range of ratios of canopy height to clear alleyway spacing. With apple canopies, a ratio between actual light interception and \(F_\mathrm{max}\) may be more useful. If this ratio exceeds 0.7 then self-shading is probably excessive.

Overall effects of shade on fruit quality are very clear, but processes responsible are not so clear. Shade reduces PAR and, therefore, local photosynthetic activity; but canopy shade also reduces temperature (Greer and Weedon 2012) and changes wavelength distribution of transmitted light. Leaves absorb strongly in the visible part of the spectrum (400–700 nm), but have a high transmittance and reflectance to wavelengths in the near infrared (see Figure 12.1 at start of this chapter). This difference in light quality between incident and transmitted sunlight is usually expressed as a red/far-red ratio, that is, a ratio between irradiance around 660 nm compared with 730 nm wavebands. These wavebands correspond to peaks of absorption by phytochrome (Chapter 8), and are strongly implicated in developmental responses to canopy shade. Correlated changes in irradiance and the red/far-red ratio of canopy light make it difficult to separate the effects of changing irradiance from the effects of a change in the red/ far-red ratio, but it is likely that changes in berry composition are due to combined effects of irradiance and red/far-red ratio.

Due to the perennial nature of fruit trees, environmental conditions in one season can have carry-over effects on growth and development during the subsequent season. In seasonally deciduous trees and vines, flowers that emerge each spring were actually initiated during the previous growing season, and conditions prevailing at that time will have influenced the extent and intensity of flower bud differentiation. In temperate horticulture, flower initiation is not a continuous process but may be restricted to several weeks during mid to late summer, followed by several months of continuing development before passing into dormancy over winter. Floral development is then completed during the following spring ahead of flower emergence. In addition to changes in fruit quality of current crops, canopy shade during summer will also reduce flower bud initiation and differentiation.

Flower bud reduction due to shading seems to be a general phenomenon in perennial fruit crops and has been reported for apple, pear, apricot, peach, coffee, cacao and grape. With grape, the number and size of cluster primordia generally increases with increasing light. In this case, plants are responding to light quantity rather than quality (expressed as changes in the red/far-red ratio). Cultivars differ in their response to shade. Sultana (syn. Thompson Seedless) requires approximately 30% full sun for cluster initiation compared to 10% for Rhine Riesling. Timing of shading is also important for grapes. Shading in the period during bud development of grape in late spring has the greatest negative effect on flower initiation.

In citrus, shading may not of itself reduce flowering but can induce heavy fruit abscission. Similarly, shading whole apple trees 14–28 d after full bloom can result in very heavy fruit loss. Two days shading with shade cloth transmitting 8% light was sufficient to reduce fruit set by 80% (Byers et al. 1991). So effective is this treatment that deep shade could work as a non-chemical fruit thinner! In sour cherry, fruit set is adversely affected by light levels within the canopy below 20%, and flower bud initiation requires an irradiance of 15–20% full sun. Shading of whole vines or shoots of kiwifruit during summer can reduce flowering the following spring. Again, as with grapes, changes to the red/far-red ratio did not alter the flowering response of kiwifruit vines to total irradiance. Yields of kiwifruit vines next to shelterbelts are significantly lower than those from vines in the centre of fruit blocks, due presumably to a reduction in flowering as a result of shade from the shelterbelt. This can depress yield by two thirds.

While shading generally reduces fruit quality, excess solar radiation can lead to serious downgrading of fruit quality. Apples, grapes and kiwifruit suffer from sunburn, particularly where the fruit has been growing in the shade and then is thrust into full sunlight by movement of branches due to weight of fruit or to summer pruning or defoliation removing foliage that previously shaded the fruit. This tends to be a much larger problem in regions of high solar radiation receipt than cloudy areas.

Perennial fruit orchards do offer great potential for modification of light and temperature environments within canopies by pruning, tree training, tree size, row spacing and row orientation. Because of the great variety of ways of arranging the foliage in space, a number of models have been written to examine the relative importance of some of these factors in influencing not only light interception (Table 12.1) but also sunlight distribution within the canopy (Palmer 1989; Wagenmakers 1991), as this can have such a profound effect upon the quality of the fruit as already outlined.

In addition, field experiments to examine these effects are very expensive and time consuming to set up and run, so models offer a very economical way of examining light interception and distribution within innumerable canopy forms. As there is often a large dollar premium for quality, the economic success of any production system is largely determined by the yield of high-quality fruit, rather than the total yield. That does not mean, however, that high total yield and high-quality yield are mutually exclusive. With grapevines, Smart (1989) has consistently argued that high yields of high-quality grapes are achievable via correct canopy management.

Highly productive orchards and vineyards, therefore, have a balance of vegetative and reproductive growth, with fruiting zones maintained in a high light environment. Examples of how this has been achieved will now be presented for apples, peaches and grapes. In each case only one system is described, although there are many other successfully managed systems, particularly in vineyards.

(a)  Apples

In New Zealand, Tustin et al. (1990) have sought to combine requirements for precocity, high yields of high-quality fruit and good light penetration into the canopy in their slender pyramid tree form. This has been developed with trees on semi-vigorous rootstocks at a tree density of about 700 trees per hectare. The form is basically a central leader tree, that is, one central vertical trunk, on which are borne the fruiting branches. Early tree management is aimed at developing a permanent, strong, spreading basal tier of four to five branches emanating from the central leader at wide angles for strength and to encourage early fruiting. Pruning is minimal in the early years, with unwanted shoots being removed during the growing season when they are still small. The upper part of the tree is developed as an open, well-spaced arrangement of whorls of shorter branches arising directly from the central leader. These upper branches are removed when they become too large or pendulant and are replaced by natural regrowth. Each tree is maintained in an overall pyramidal form to encourage light penetration into all parts of the canopy. Yields of Royal Gala apples, for example, have been over 50 t ha^–1 in the third year rising to over 100 t ha^–1 by year six.

(b) Peaches

Trees on a Tatura trellis (Figure 12.27) are trained into two planar canopies inclined at an angle of 60º from the horizontal, and held by a trellis system of posts and wires. The system is designed to encourage precocity by using 2,000 trees per hectare and rapidly filling the trellis structure with fruiting branches. Within each arm, the canopy itself is shallow to encourage good light penetration. Summer pruning of unwanted, upright vegetative growth is practised to maintain a high, uniform light interception environment along each arm. Vegetative growth has also been successfully controlled in the dry environment of Tatura by regulated deficit irrigation.

The Tatura trellis is also designed for mechanical picking. A rigid and shallow canopy ensures that fruit can fall onto the catching frame with minimal chance of damage. As peaches bear fruit on one-year-old wood, yields of Golden Queen on Tatura trellis in year two have reached 28 t ha^–1 rising to a maximum of 86 t ha^–1 by year four (van den Ende et al. 1987). Other stonefruit and pomefruit (pipfruit) have also been grown successfully with this management system.

(c) Grapes

Traditional pruning of grapevines was aimed at producing a limited number of moderate-sized clusters of berries to facilitate hand picking. Consequently, pruning removed large amounts of young wood so that growth of vigorous shoots was stimulated. With the advent of mechanical picking for wine grapes, however, this constraint has been removed as the harvesters are capable of efficiently removing the berries from large and small grape bunches. This has consequently brought about new grapevine pruning and training techniques, particularly in regions with long growing seasons, irrigation and high vigour such as Australia, Chile and California.

Minimal pruning of cordon-trained vines (MPCT) is one such example from Australia. Each vine is initially developed conventionally with two or four permanent horizontal arms or cordons. From year three, vines are minimally pruned — low hanging canes are removed. Consequently MPCT vines carry far more buds over from one year to the next, but competition between these growing points results in shorter shoots, with shorter internodes, and higher yields made up of a large number of small clusters of berries well exposed to the light. The resulting wine quality is high and comparable with that from conventionally pruned vines.

Investigations of UV effects on plant biology largely depend on the use of UV-B emitting lamps in both laboratory and field. Interpretation of results from such systems is, however, restricted by an inability to mimic the solar spectrum precisely (Figure 12.31). As a consequence, comparisons between species with respect to UV-B sensitivity, and analyses of processes responsible for variation in sensitivity, must be treated circumspectly. Despite these methodological limitations, overall outcomes are unambiguous: UV-B radiation impacts on many aspects of plant biology, as reviewed by Tevini (1994) and Bornman and Teramura (1993).

(a) Growth and development

Sensitivity to UV-B irradiation includes any morphological, physiological or biochemical change induced by UV-B. Significant effects have been reported for about half of the 300 or so crop species and cultivars studied so far, with some species more susceptible than others (Table 12.2). Sensitivity is noticeable in plant growth and development. Reduction in leaf area, stem growth (stunting) and total plant biomass are commonplace. Additional symptoms include bronzing and glazing of leaf surfaces.

Growth reductions depend not only on the level of UV-B exposure but on the associated photon irradiance. Partitioning of growth to different organs, for example altered internode length, or leaf production, is also sensitive to UV-B irradiation. Such morphological changes may not be significant to plants in isolation but may influence competitive interactions, and especially their competition for sunlight. Sensitivity to UV-B irradiation also varies with life cycle. Seedlings are especially vulnerable, as are mature plants under-going their transition from vegetative growth to reproductive development.

(b) Cell physiology

Several sets of processes at both cellular and molecular levels which are critical to plant growth and reproductive development appear to be affected by absorption of UV-B radiation. Especially prominent are photosynthesis, signal transduction and nucleic acid metabolism.

In general, UV-B radiation causes a net inhibition of photosynthesis in a wide range of plants. From laboratory studies, this inhibition appears to arise from disruptions at a number of points in the photosynthetic cycle, including disruption of PSII reaction centres (Strid et al. 1990), a decrease in Rubisco activity and damage to photosynthetic pigments (chlorophylls and carotenoids). Stomatal function, and thus leaf gas exchange, is also commonly impaired.

Alterations in plant growth induced by UV-B radiation have been partly attributed to changes in nucleic acid structure and function (Tevini 1994). DNA absorbs strongly in the UV region and is thus especially prone to damage by UV-B radiation (Figure 12.31). The most common lesions are breaks in DNA chains, with a resultant production of thymine dimers. They in turn interfere with accurate base pairing, leading to a disruption of transcription and replication of DNA (Stapleton 1992). These disruptions amount to a mutagenic action for UV radiation in many organisms. Proteins and RNA can also absorb UV-B and are inactivated as a result, but this loss is of secondary importance due to their relative abundance compared with DNA (Stapleton 1992).

Activation and photo-deactivation of important signal molecules, such as hormones and photoreceptors, may also compound effects of UV-B irradiation on plant growth and development. For example, cell extension in many plants is influenced by indole acetic acid (IAA) which absorbs in the UV-B region and is photo-oxidised to 3-methyleneoxindole, an inhibitor of hypocotyl growth when exogenously applied. In contrast, irradiation with UV-B can induce enzyme activity in the shikimic acid pathway, which regulates the synthesis of a broad array of plant compounds, ranging from flavonoids to lignin, all of which are important to plant function, including tolerance to UV-B radiation.

(c) Reproduction

Flowering, pollination and seed development are variously affected by UV-B irradiation. Flowering appears to be disrupted by UV-B radiation by decreases in flower number and alteration in timing reported in the few species so far studied. Such effects may have important consequences for natural plant populations, which rely on the synchrony of flowering with the presence of appropriate insect pollinators.

Although pollen appears resilient to UV-B radiation damage, owing to high levels of flavonoids in the anthers and pollen wall, germinating pollen tubes are highly sensitive to UV radiation and suffer from large decreases in growth rate. Such disruption can lead to lowered fertilisation success and decreases in seed yield.

(d) Ecology

Genetic variation in sensitivity to UV-B radiation has implications for plant competition and thus plant ecosystem dynamics and community structure, in both natural and managed ecosystems. Competition between agricultural crops and associated weeds may be altered under enhanced UV-B irradiation. In the few studies considering the impact of UV-B irradiation on natural plant communities, most notable is the work of Caldwell et al. (1982). They found arctic plant species were much more sensitive to UV-B, both in terms of growth and reproduction, than alpine species. Arctic species grow under a naturally low UV-B environment, whereas alpine species grow under a naturally high UV-B environment by virtue of higher altitude. Arctic plant communities could thus be altered to a greater extent than alpine communities by any substantial rise in natural UV-B.

(e) UV-B tolerance mechanisms

Many organisms have evolved mechanisms to undo the molecular damage caused by UV radiation. Possibly the most adaptive are terrestrial plants that rely on full sunlight for photosynthesis. Protective mechanisms can be classified into two main classes: (1) those whereby UV damage is repaired or its effects negated or minimised, and (2) those whereby the amount of UV radiation actually reaching sensitive areas is reduced. While protective in nature, all of these mechanisms impose an energy cost on plants so adapted.

For the first class of protective mechanism, organisms have developed three important repair processes for UV-induced DNA damage (Stapleton 1992): photoreactivation, excision and repair of DNA, and post-replication repair. Photoreactivation is the light-induced enzymatic process which cleaves pyrimidine dimers formed by UV radiation — thus restoring proper base pairing. Excision and repair of DNA involves the excision of UV photoproducts from DNA molecules (this mechanism requires no light energy and uses undamaged DNA templates as a guide). Post-replication repair occurs where DNA lesions are bypassed during DNA replication and information from the sister duplex is later used to fill gaps.

As mentioned above, plant growth and development is slowed by exposure to enhanced UV-B radiation. Such delay also minimises adverse effects from damage that has occurred. Growth delay and slower cell division provides additional time for DNA repair mechanisms to operate ahead of any recommencement in DNA replication.

Screening sensitive tissues from UV-B radiation is a secondary option available to plants either to avoid or at least minimise damage. Tissue screening may be achieved through structural modification of organs or by screening molecules which absorb UV radiation. Such features may be either static, as with leaf orientation or phototaxis, or dynamic, as in synthesis of screening molecules which absorb UV radiation in a highly selective way. Screening molecules commonly appear after exposure to UV radiation as secondary metabolites such as flavonoids. Substantial amounts of such pigments accumulate especially in the upper epidermis of leaves. Along with cuticular waxes and other cellular components, these substances attenuate incident UV radiation, and energy transmitted to underlying tissue is decreased by up to two orders of magnitude (Figure 12.33). Typically less than 1% of incident UV-B radiation reaches the lower epidermis. None is transmitted through an entire leaf. Flavonoid pigments are synthesised by leaves on many plants in direct response to UV radiation.

(f) Environmental interactions

Field-grown plants are subject to variable environmental conditions during their life cycle. In their extremes, such factors can lead to stresses such as water stress, mineral stress, temperature stress, disease and stresses due to anthropogenic pollution (ozone, acid rain). The interaction of UV-B irradiation stress with other environmental factors has been examined in only a few cases, essentially because of the difficulty of simulating elevated UV-B irradiation in the field. Of the environmental interactions studied, water stress appears to influence plant responses induced by UV-B irradiation. In soybean, for example, a decrease in yield in sensitive cultivars under elevated UV-B irradiation was most apparent under well-watered conditions. Water deficit in combination with elevated UV-B irradiation did not reduce yield to a greater extent than water deficit alone. Water stress may, therefore, mask UV-B responses of plants.

Elevated CO₂ levels may also modify the response of sensitive plants to UV-B irradiation. In rice and wheat (but not in soybean) an increase in seed yield and biomass under elevated CO₂ was reversed under moderate levels of supplementary UV-B irradiation.