The inhibition of photosynthesis at high light intensities must be taken into account in ecological studies, since the intensities typically experienced in the surface layer of natural waters in sunny weather are in the range that can produce photoinhibition. Indeed if the depth profile of phytoplankton photosynthetic activity is measured by the suspended bottle method in inland or marine waters, a noticeable diminution in the specific photosynthetic rate or the rate per unit volume is commonly, although not invariably, observed near the surface. Figure l0.4 shows examples of this surface inhibition of photosynthesis in a coastal and an inland water. With increasing depth and diminishing light intensity, photoinhibition lessens and the maximum, light-saturated but not inhibited, photosynthetic rate is achieved. With further increase in depth, irradiance falls to the point at which light intensity becomes limiting and from here on the photosynthetic rate diminishes roughly exponentially with depth approximately in parallel with irradiance.

Many, but not all, macrophyte species also show inhibition of photosynthesis when exposed to light intensities in the range of full sunlight, fldtE of phoiflivn Uliesia (rug C m"* h"L> 0 20 40 60 BO 10O 120

fldtE of phoiflivn Uliesia (rug C m"* h"L> 0 20 40 60 BO 10O 120

Fig. 10.4 Depth profiles of phytoplankton photosynthetic rate per unit volume of water. The curves are for an inland water (Lake Windermere, England; plotted from data of Belay, 1981, assuming a photosynthetic quotient of 1.15), and a coastal water (Bedford Basin, NS, Canada; plotted from data of Marra, 1978).

Fig. 10.4 Depth profiles of phytoplankton photosynthetic rate per unit volume of water. The curves are for an inland water (Lake Windermere, England; plotted from data of Belay, 1981, assuming a photosynthetic quotient of 1.15), and a coastal water (Bedford Basin, NS, Canada; plotted from data of Marra, 1978).

and this is especially the case for algae taken from greater depths.517,1162 Ecologically, however, this phenomenon is of less significance since any given macrophyte species is generally to be found growing at a depth where the light intensity is one to which it is well adapted (Chapter 12), whereas phytoplankton are circulated within a range of depths by water movement. Some photoinhibition nevertheless sometimes occurs in macrophytes in shallow waters in the middle part of the day.517 Marine macrophytic algae of the intertidal zone are intermittently exposed to very high light intensities. At irradiance values equivalent to full sunlight some of these species show no inhibition, but others are partially inhibited.691 In the coral, Stylophora pistillata, in the Gulf of Aqaba (Red Sea), Winters et al. (2003) using in situ PAM fluorescence measurements, found a marked midday depression (63%) of effective quantum yield in coral growing at 2 m depth, but only an 8% depression in coral growing at 11 m.

Inhibition of photosynthesis by high light intensities takes time to develop. In the case of phytoplankton populations from Lake Ontario, Canada, the decline in photosynthetic activity began after about 10min exposure.537 Measurements of the time course of photosynthesis by populations of the diatom Asterionella in bottles suspended at the surface of a Welsh lake indicated that the inhibitory effect was small during the first hour but became significant during the second hour.91 The higher the temperature at a given light intensity, the more rapidly inhibition ensues.537 In the case of laboratory cultures of Asterionella grown at 18°C and 200 mmolphotonsm-2s-1, exposure to 2000 mmolphotonsm-2s-1 full sunlight) for 1 h at 18° and 25°C reduced the subsequently measured photosynthetic rate by about 10 and 50%, respectively.92

Phytoplankton can recover from the inhibitory effects of intense light if they are transferred to a lower light intensity.470 The longer the exposure to bright light, the longer the recovery takes. In the case of Asterionella populations from a Welsh lake, recovery from 2h exposure to bright sunlight was complete after 4 h in low light intensity: after 6 h bright sunlight, which reduced photosynthetic rate by 70%, recovery took 20 h.91

The mechanism of photoinhibition has been studied in most detail in higher plants. Jones and Kok (1966) measured the action spectrum of photoinhibition of electron transport in spinach chloroplasts. The spectrum showed its main activity in the ultraviolet (UV) region with a peak at 250 to 260 nm. Photoinhibition also occurred in the visible region but with a very much lower quantum efficiency. Between 400 and 700 nm, the action spectrum followed the absorption spectrum of chloroplast pigments, with a distinct chlorophyll peak at 670 to 680 nm. The lesion appears primarily to affect the light reactions of photosynthesis by damaging the reaction centre of photosystem ii.265,266,230

The shape of the action spectrum in the UV region suggests that plastoquinone or some other quinone functional in the reaction centre may be the sensitive molecule so far as UV inhibition is concerned. The primary site of damage to the photosynthetic system by UVB appears to be photosystem II, suggesting that it is QA, the quinonoid primary electron acceptor of photosystem II that is the crucial target. The shape of the action spectrum in the visible region indicates that at very high light intensities some of the energy absorbed by the photosynthetic pigments themselves is transferred to a sensitive site - not necessarily the same site as that affected by UV - where it causes damage.

Although detailed studies on the basis of photoinhibition of algal photosynthesis have not been carried out, the most plausible and economical hypothesis is that the mechanism is the same as in higher plants. For oceanic phytoplankton, the observed photoinhibition was found to vary linearly with the daily biological dose calculated using the Jones and Kok action spectrum.1247 In the surface layer of clear ocean waters, 50% of the photoinhibitory dose is at wavelengths less than 390 nm; in moderately productive waters (0.5mgchl am~3) at 10 m depth, 50% of the photo-inhibitory dose is at wavelengths less than 430 nm.1243 Thus, for oceanic waters we may attribute about 50% of the photoinhibition to UV and about 50% to visible light. Field measurements by Smith et al. (1992) in the Bellingshausen Sea in the austral spring of 1990 indicated that primary production in the Antarctic marginal ice zone was 6 to 12% inhibited by the increased UV flux resulting from ozone depletion. In the giant kelp, Macrocystis pyrifera, Clendennen et al. (1996) found that doses of UV that reduced photosynthesis by 50% caused a substantial reduction in the number of functional photosystem II centres, and impaired energy transfer from antenna pigments (fucoxanthin, chlorophyll a, chlorophyll c) to photosystem II, but had no effect on photosystem I, indicating that in this phaeophyte species, as in spinach, photosystem II is the primary site of damage. The 32kDa D1 protein of photosystem II, which contains the QB plastoquinone-binding site, undergoes continuous rapid turnover in the light, at a rate which increases with light intensity. Greenberg et al. (1989) found that the quantum yield for degradation was highest in the UVB region of the spectrum, suggesting that enhanced breakdown of this protein may be involved in the sensitivity of photosystem II to UV.

Glacial lakes at higher latitudes, which were formed following the retreat of the glaciers at the end of the last Ice Age, ~10 700 years ago, did not acquire tree cover in their catchments for many centuries, and consequently lacked the supply of dissolved organic matter, with its associated colour, which tree leaves provide. On the basis of palaeoeco-logical analysis (fossil algal pigments, organic matter content) of the sediments of lakes in British Columbia, Canada, Leavitt et al. (2003) concluded that algal abundance was depressed ten-fold by UV radiation in the first millennium of lake existence.

Over the course of evolution, some aquatic plants have acquired a degree of protection against UV in the form of the mycosporine-like amino acids (MAAs, Chapter 3), compounds that absorb in the UV with peaks in the 300 to 360 nm region. Their distribution in marine organisms has been reviewed by Shick and Dunlap (2002). They occur in both prokaryo-tic and eukaryotic phytoplankton, but not all species possess them. Bloom-forming dinoflagellates have a particularly high capacity to form MAAs, and the cellular concentration is many-fold greater in cells grown at high light than in low light.978 Some diatom species do not accumulate these compounds. Five species of Antarctic diatom in culture showed little or no ability to synthesize MAAs, even when exposed to high levels of UV, in contrast to the Antarctic prymnesiophyte, Phaeocystis, which does form these compounds.281 The marine cyanobacterium, Trichodesmium, which forms extensive surface blooms in oligotrophic tropical and subtropical seas, and which is consequently exposed to intense solar radiation, contains particularly high levels of MAAs, among the highest known for free-living phytoplankton.1319 Among the macro-phytes, MAA synthesis is common among the Rhodophytes, but less so among Chlorophytes. Some deep-water red algal species, which would not normally encounter UVB, lack the ability to make MAAs.590 Phaeo-phytes do not synthesize MAAs, but may not need to since brown algae contain UV-absorbing phenolic compounds: in the intertidal brown alga, Cystoseira tamariscifolia, in southern Spain, Abdala-Diaz et al. (2006) found the level of phenolic compounds in the thallus to increase about four-fold as daily integrated irradiance increased from February to June, and then to decrease by nearly 50% as irradiance decreased from June to November. In those algae that can make MAAs, there is a general tendency for the amounts formed to increase with UV exposure. In coral reefs the concentration of MAAs within the coral colonies decreases with depth.337

Aquatic yellow substances absorb strongly in the UV. We may therefore expect photoinhibition to be less apparent in the more coloured waters: this has been observed to be the case in highly productive tropical oceanic waters with high levels of gilvin.735 By the same token it seems likely that photoinhibition in the more highly coloured (i.e. most inland) waters is caused mainly by the visible (400-700 nm) component of the solar radiation.

In addition to that photoinhibition which is due to direct damage to the reaction centres, and which takes some hours to repair, there is another kind which comes into operation very quickly in intense light, and which is reversed relatively quickly (in a matter of minutes rather than hours) in the dark. This process, which involves reversible changes in the carotenoid composition of photosystem II, referred to as the xantho-phyll cycle,1482,303,1021 can be regarded as a useful adaptive response of the photosynthetic system to excessively intense light rather than a symptom of internal damage. In higher plants and most members of the Chlorophyta, and in the Phaeophyta, one of the antenna pigments feeding energy to the reaction centre of photosystem II is the diepoxide carotenoid, violaxanthin. When the photosystems are absorbing light energy at a rate approaching the maximum at which the photochemically generated electrons can be used for CO2 reduction, the internal pH of the thylakoid lumen falls markedly. This activates the enzyme, violaxanthin de-epoxidase, which removes first one of the epoxy O atoms, to give the monoepoxide, antheraxanthin, and then removes the other to give the non-epoxide carotenoid, zeaxanthin. Energy absorbed by zeaxanthin is not transferred to the photosystem II reaction centre and is, instead, dissipated as heat. When the cells are transferred to the dark, the intra-lumenal pH rises and a different enzyme, an epoxidase, is brought into play, which brings about the oxidation of zeaxanthin, by the addition of two epoxy O atoms, reconverting it to violaxanthin. In non-green algae, xanthophyll cycles that make use of other carotenoids occur. For example, in the Bacillariophyceae, Chrysophyceae, Haptophyceae and Euglenophyta, interconversion takes place between the monoepoxide, diadinoxanthin (Fig. 8.12/), and the non-epoxide, diatoxanthin.

In the algae generally, both phytoplankton and benthic, the proportion of total xanthophyll existing in the photosynthetically non-functional, photoprotective form, such as zeaxanthin, increases with the light intensity in their environment, and changes with ambient irradiance during the day. In the case of the floating pelagic phaeophyte, Sargassum natans, in the gulf of Mexico, Schofield et al. (1998) found that the violaxanthin: zeaxanthin ratio fell from at 04:00 h to at midday, and then rose again to by 22:00 h. The microphytobenthos of tidal mudflats adjusts the state of its xanthophyll pool when it becomes exposed to full sunlight at low tide. In the mudflats of the estuary of the River Barrow (Ireland), where the microphytobenthic community is dominated by diatoms, Van Leeuwe et al. (2008) found that whereas diatoxanthin could hardly be detected at 09:00 h immediately after emersion, the diatoxanthin/(diato-xanthin + diadinoxanthin) ratio had risen to ^0.2 at 10:00 h, and reached its maximum value of just over 0.3 at midday. In phytoplankton populations from a large number of stations in the Arabian Sea and coastal waters around Vancouver Island (Canada), Stuart et al. (1998) found a strong inverse relationship between the proportion of non-photosynthetic carotenoids, such as zeaxanthin and diatoxanthin, and the chlorophyll concentration, suggesting that the small cells that are characteristic of oligotrophic waters have a higher proportion of photoprotective xantho-phyll pigments. In phytoplankton sampled from depths between 5 and 75 m in the NW Atlantic Ocean near the continental shelf break, Prieto et al. (2008) found a significant positive correlation between the proportion of photoprotective carotenoids and the irradiance of PAR to which the cells were exposed at the time of collection.

Depth profiles of phytoplankton photosynthesis, such as those in Fig. 10.4, determined by the suspended bottle method, tend to overestimate the extent to which photoinhibition diminishes primary produc-tion.537,867,855 In nature the phytoplankton are not forced to remain at the same depth for prolonged periods. Some, such as dinoflagellates and blue-green algae, can migrate to a depth where the light intensity is more suitable (see §12.6). Even the non-motile algae will only remain at the same depth for extended periods under rather still conditions. Wind blowing across a water surface induces circulatory currents known as Langmuir cells, after the eminent physical chemist, Irving Langmuir, who first studied them.765 Langmuir cells are horizontal tubes (roll vortices) of rotating water, their axes aligned approximately parallel to the wind direction (Fig. 10.5). Adjacent tubes rotate in opposite directions and tubes of varying diameter can be present at the same time. The simultaneous occurrence of both wind and waves is necessary for the generation of these roll vortices,386 but even a light wind over small-amplitude waves can set them going. Cells can have diameters ranging from a few centimetres to hundreds of metres: with a wind speed of 5 m s-1, a typical cell might have a diameter of 10 m and a surface speed of 1.5cms-1.371 Measurements by Weller et al. (1985) from the research platform FLIP, drifting off the coast of southern California, showed that with quite moderate wind speeds (mainly 1-8 ms-1), downwelling flows typically between 0.05 and 0.1 m s-1 were generated. The mixed layer above the seasonal thermocline was at the time about 50 m deep, and the strongest downwelling flows were observed between 10 and 35 m depth, corresponding to the middle region of the mixed layer. Above and below that region, downwelling flows were generally less than 0.05m s-1), and there appeared to be no downwelling flow in or below the seasonal thermocline.

Thus it will very commonly be the case that phytoplankton are not held in the intensely illuminated surface layer but are slowly circulating throughout the mixed layer. Harris and Piccinin (1977) point out that on the Great Lakes of North America the average monthly wind speed

Wind Induced Current
Fig. 10.5 Wind-induced circulatory currents (Langmuir cells) in a water body.

throughout all the winter, and most of the summer period, is sufficient to generate Langmuir cells, and that the residence time at the surface under such conditions will not be long enough for photoinhibition to set in. Within any given month of course, although the average wind speed may be enough to ensure Langmuir circulation, there will be calm periods in which it does not occur. Phytoplankton sampled in winter from the waters of Vineyard Sound (Massachusetts, USA) showed marked photoinhibition in bottles held at surface light intensities, but were in fact well adapted to the average light intensity that they would actually encounter in this well mixed shallow coastal water.462

Photoinhibition of phytoplankton is only likely to be of frequent significance in water bodies in which high solar irradiance commonly occurs together with weak wind activity, leading to the formation of transient shallow temperature/density gradients in the surface layer that impede mixing and thus trap phytoplankton for part of the day in the intense near-surface light field. A well-documented example is the high-altitude (3803 m), low-latitude (16° S) Lake Titicaca (Peru-Bolivia). Vincent, Neale and Richerson (1984) found the typical pattern of thermal behaviour to be that a near-surface thermocline began to form each morning, persisted during the middle part of the day, and was then dissipated by wind mixing and convective cooling towards evening and through the night. While the near-surface stratification persisted, phytoplankton photosynthesis in the upper layer was strongly depressed. That this was not an artifact resulting from phytoplankton immobilization in bottles was shown by the observation that the cellular fluorescence capacity (believed to correlate with the number of functional photosystem II complexes) of phytoplankton samples taken from the water was also greatly reduced. Neale (1987) estimated the diminution of total water column photosynthesis in L. Titicaca on such days to be at least 20%. Elser and Kimmel (1985) have also used measurements of cellular fluorescence capacity to show that in reservoirs in temperate regions (southeastern USA) photoinhibition does occur in the surface layer under calm sunny conditions.

On balance we may reasonably conclude that photoinhibition of photosynthesis in the surface layer, although it exists, is not as frequent a phenomenon as was originally thought. It can significantly reduce areal photosynthesis under sunny, still conditions, but is likely to be of small or no significance when there is even a light wind. Underestimates of primary production resulting from the use of stationary bottles are likely to be more serious in oligotrophic waters requiring long incubation times than in productive waters. It should be noted, however, that circulation does not by any means always increase primary production: as we shall discuss more fully in the next chapter, circulation through too great a depth can diminish total photosynthesis by keeping the cells for significant periods in light intensities too low for photosynthesis.

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