Against the background of environmental variability, there may be superimposed variations in the contemporary ambient range of fluctuations, subjecting hitherto supposedly acclimated plank-ters to additional demands of accommodation. Among the most crucial of these is a weakening of the mechanical forcing, either as a result of a sharp reduction in the wind speed or of sharp increase in the photon flux (perhaps as the cloud clears) or, as is often the case, the coincidence of both events. In all these instances, the abrupt shortening of the Monin-Obukhov length is, far from being the net beneficial influence cited above (in Section 3.3.3), potentially highly dangerous. Part of the hitherto entrained population becomes disentrained deep in the water column, where the irradiance is markedly sub-saturating. Another is retained within a new, much shallower, surface circulation, exposed to a much elevated I* value and to a probable excess of radiation in the harmful, high-energy ultraviolet wavelengths. The greater the previous adaptation to low average insolation and the more enhanced is their light-harvesting capacity then, clearly, the greater is the danger of damage to the cells affected. Analogous risks confront plankters near the surface of lakes becalmed overnight and subject to rapid post-dawn increases in insolation. In a lesser way, perhaps, even short bursts of strong light on a mixed layer or lulls in the wind intensity acting on turbid water under bright sunshine will result in potentially sharp increases in the photon flux experienced by individual algae. Moreover, this is the fate of isolates of wild populations, sampled from the water column, sub-sampled into glass bottles and then held captive at the top of the water column; it is little wonder that their performance becomes impaired (Harris and Piccinin, 1977) (see Section 3.3.1).
In fact, photoautotrophic plankters are equipped with a battery of defences for coping with and surviving exposure to excessive solar radiation levels. As has already been said, some of these have the effect of cutting photosynthetic rate and the response was formerly interpreted as 'photoinhibition'. Strong light certainly can inhibit photosynthesis and do a lot of physical damage to the photosynthetic apparatus. However, many of the observed responses are pho-toprotective and serve to avoid serious damage occurring to the cell. These are reviewed briefly below; the sequence is more or less the one in which live cells, suddenly confronted by supersaturating photon fluxes, invoke them in response. Some excellent, detailed reviews of this topic include Neale (1987), Demmig-Adams and Adams (1992) and Long et al. (1994).
In simply moving upwards from a sub-saturating light to a depth where the photon flux density supersaturates not just the demand for growth but also the carbon-fixing ability of PSI, the entrained cell will experience two almost concurrent effects, evoking two compounding reactions. The greater bombardment of the LHCs by photons means that some of these now arrive at reaction centres that are still closed, pending reoxidation of the acceptor quinone, QA (see Section 3.2.1). At the same time, the accelerated accumulation of PQH2 in the plastoquinone pool slows the re-reduction of P680 and, hence, the reactivation of the LHCs. The energy absorbed from unused photons continuing to arrive at P680 is re-radiated as fluorescence. This is readily measurable: the spectral signal of emitted fluorescence has long been used as an index of plankton biomass (an analogue of an analogue: Lorenzen, 1966). Differences in the spectral make-up of the emission can also be used to separate the organis-mic composition of the phytoplankton, at least to the phylum level (Hilton et al., 1989). However, because the transfer of electrons from the plas-toquinone pool to PSI is a rate-limiting step, the size of the PQ pool is a measure of the photo-synthetic electron transport capacity. In this way, PSII fluorescence may also be exploited as a sensitive analogue of photosynthetic activity (Kolber and Falkowski, 1993). Light-stimulated in vivo fluorescence from cells exposed to a flash of weak light in the dark (F0, when all centres are open) is compared with the fluorescence following a subsequent saturating flash (Fm, corresponding to their total closure). The presence of open centres quenches the fluorescence signal proportionately, so the difference, (Fv = Fm — F0), becomes a direct measure of the photosynthetic electron-transport capacity available and the extent of the reduction in the quantum yield of photosynthesis caused by exposure to high light intensities.
As a relatively short-term response, the chlorophyll-a fluorescence yield alters as the plankters are moved up and down through the mixed layer. The measurement of fluorescence to investigate the transport and the speed of photoadaptive and photoprotective reactions of phytoplankton to variable underwater light climates is one of the exciting new areas of applied plankton physiology (Oliver and Whittington, 1998).
Provided they are adequately disentrained and their intrinsic movements are adequately effective, motile organisms migrate downwards from high irradiance levels. Avoidance reactions have been observed especially among the larger motile dinoflagellates (see, especially, Heaney and Furnass, 1980a; Heaney and Talling, 1980a)
and larger, buoyancy-regulating Cyanobacteria (Reynolds, 1975, 1978b; Reynolds et al., 1987). For non-motile diatoms, a rapid sinking rate may provide an essential escape from near-surface 'stranding' through disentrainment, especially in low-latitude lakes. The relatively high sinking rates in (especially) Aulacoseira granulata may be a factor in the frequency of its role as dominant diatom in many tropical lakes where there is a diel variation in mixed water depth (see Reynolds et al., 1986). The effect may be significantly enhanced by spontaneous acceleration of the sinking rate of cells coping with an abrupt increase in insolation (Reynolds and Wiseman, 1982; Neale et al., 1991b), perhaps as a result of the withdrawal of the alleged mechanism of vital regulation (see Section 2.5.4).
Planktic cells are generally too small for plastid relocation to have the significance it does in the cells of higher plants (Long et al., 1994) but, over periods of minutes to hours of exposure to high light intensities, contraction of the chro-mophores of planktic diatoms lowers the cross-sectional areas projected by the cell chlorophyll (Neale, 1987).
In cells exposed to frequent or continuing high light intensities over a generation time or more, over-excitation of the PSII LHCs is avoided by changes affecting the xanthophylls. These oxygenated carotenoids are subject to a series of light-dependent reactions, which, among the chlorophytes (as among green higher plants), results in the accumulation of zeaxanthin under excess light conditions and its reconversion to violoxanthin on the return of normal light conditions. Among the dinoflagellates and the chrys-ophyte orders (sensu lato, here including the diatoms), an analagous reaction involves the conversion of diadinoxanthin to diatoxanthin, when light is excessive, with oxidation back to diadi-noxanthin in darkness. The reaction is said to be about 10 times faster than the analogous reaction in higher plants (Long et al., 1994, quoting the work of M. Olaizola). The principal func tion of the xanthophyll cycle in protecting PSII from excessive photon flux density operates by siphoning off a good part of the energy as heat. Many details of the cycle and its fine-tuning are considered by Demmig-Adams and Adams (1992). Here, it is important to emphasise how these adaptations of phytoplankton to high light assist in maintaining photosynthetic productivity. Carotenoids are especially effective in protecting cells against short-wave radiation and the risk of photooxidative stress.
Compounds specific to the absorption of ultraviolet wavelengths, previously known from the sheaths of epilithic mat-forming Cyanobacteria of hot springs (Garcia-Pichel and Casten-holz, 1991), where they screen cells from damaging wavelengths of radiation (max absorption ~370nm), have been found recently in the natural phytoplankton of high mountain lakes. Laurion et al. (2002) suggested that, together with the carotenoids, these mycosporine-like amino acids may occur widely among limnetic phytoplankton species, especially in response to exposure to ultraviolet wavelengths. Ibel-ings et al. (1994) demonstrated just this sort of acclimation of planktic species, especially in Microcystis, where the sustained presence of zeaxanthin contributes to an ongoing ability to dissipate excess excitation energy as heat. As originally proposed by Paerl et al. (1983), the mechanism substantially protects cells from overexposure of surface blooms to high light.
In nutrient-limited cells, photosynthate is scarcely consumed in growth. Even under quite modest light levels, simultaneous accumulation of fixed carbon and free oxidant in the cell risk serious photooxidative damage to the cell. This is countered principally through the production of antioxidants, such as ascorbate and glutathione. High oxygen levels may trigger the Mehler reaction in PSI in which oxygen is reduced to water (Section 3.2.3). Moreover, high O2 concentrations (>400 |M) induce the oxidase reaction of RUBISCO, and the photorespiration of RuBP to phosphoglycolic acid. Release of glycolate and other photosynthetic intermediates into the water is one of the 'healthy' (cf. Sharp, 1977) ways in which cells of other algal groups regulate the internal environment by venting unusable DOC into the medium. This behaviour carries important consequences for the structure and function of pelagic communities (see Section 3.5.4).
Nevertheless, prolonged exposure of phytoplank-ton cells to high light intensities over periods of days to weeks usually results in pigment loss, loss of enzyme activity, photooxidation of proteins and, ultimately, death. Such dire consequences to the photosystems and cell structures certainly do enter the realm of severe photoinhibition and photodamage. Floating scums of buoyant Cyanobacteria are especially vulnerable to photodamage; death sequences have been graphically reported by Abeliovich and Shilo (1972). In a more recent account, Ibelings and Maberly (1998) described the loss of photosynthetic capacity in response to excessive insolation and carbon depletion in laboratory simulations of the conditions experienced in surface blooms.
At lesser extremes, the resilience of cells and opportunities for repair may allow recovery of physiological vigour. Thus, the many effects of environmental variability that can lead to a fall in the net planktic production of photosynthate, once universally labelled as 'photoinhibition', should properly be viewed as a suite of homeo-static protective mechanisms. They enable phyto-plankton to survive a large part of the full range of environmental extremes that may be encountered as a consequence of pelagic embedding (see also the discussion in Long et al., 1994).
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