Depth and shade adaptation

Given the demonstrated ability of so many phytoplankton species under laboratory conditions to increase their light-harvesting capability in dim light, especially in dim blue-green light, and given also the observed shade adaptation of natural phytoplankton populations taken from deep in the euphotic zone of stratified waters, we may reasonably conclude that ontogenetic adaptation of the phytoplankton photosynthetic apparatus to the low-intensity light field in these deep layers is a real phenomenon, although it may well coexist with phylogenetic adaptation, certain species being perhaps permanently adapted to the greater depths. We saw earlier (§11.1) that the deep phytoplankton layer makes a significant contribution to total primary production in those waters where it occurs. The shade adaptation of these phytoplankton is therefore not only relevant to our understanding of how that ecological niche comes to be filled, but is also of significance for the total primary production of the oceans. Furthermore, there is evidence for a significant enhancement of zooplankton biomass around the deep chlorophyll maximum; Ortner, Wiebe and Cox (1980) consider that this is a depth zone of particularly intense trophic activity. There is also evidence that turbulent entrainment of carbon from the base of the deep chlorophyll maximum into the bottom mixed layer can make a substantial contribution to new production.1205 Thus, when all trophic levels are taken into account these shade-adapted phytoplankton may be of even more significance for the ecology of the ocean than their contribution to primary production alone would indicate.

So far as total primary production is concerned, it is true that most of it takes place in the upper region of the euphotic zone and so, as Steemann Nielsen (1975) points out, the most relevant form of adaptation is that of the phytoplankton in the surface layer to the high irradiances prevailing there; for example, their greater ability to withstand photoinhibition. There is evidence that one of the roles of carotenoids, specifically those xanthophylls not involved in light harvesting, is to protect plants against damage by excessive light. There is also evidence that in red algae, for example, in which carotenoids contribute little to photosynthesis, the ratio of carotenoid to chlorophyll increases if the cells are grown at high light intensity.313,806 As discussed earlier (§10.2), we may reasonably assume that the acquisition of resistance to photoinhibition by phyto-plankton involves increased synthesis of protective carotenoids.

In the case of the multicellular benthic algae and angiosperms, while there is evidence for an increase in light-harvesting capacity as growth irradiance is decreased, it is less well documented than in phytoplankton species, perhaps because of the greater difficulty in culturing these plants under controlled laboratory conditions. Although more studies are required, particularly in the field, we may reasonably conclude on the basis of the information already available that in some species that grow over a range of depth, adaptation in the deeper growing individuals consists in part of an increase in pigment content per unit biomass. An alternative or additional strategy is a reduction in respiration rate; morphological changes that increase light interception by the plants may also occur.

Any adaptive ability that enables an aquatic plant species to cope with the variation in light regime over a range of depth should in principle also enable it to cope with the variation in light quality that will be found within a range of optical water types. The extent to which the ability of particular species to grow in a range of water types is due to ontogenetic adaptation of the photosynthetic apparatus has not been the subject of systematic study.

Given that a common ontogenetic response of aquatic plants to variations in light regime is to vary the light-harvesting capacity of the cells, how important is chromatic adaptation as a component of this? How important, that is, are changes in the shape of the absorption spectra (due to changes in the proportions of the pigments) of the cells, as opposed to changes in absolute absorption across the whole spectrum? In aquatic plants that do not contain biliproteins, i.e. higher plants and algae other than the Rhodophyta, Cryptophyta and Cyanophyta, changes in pigment ratios in response to changes in the ambient light are relatively small, where they occur at all. In certain green species (algae and higher plants) there is some increase in the ratio of chlorophyll b to a, during shade adaptation: this should somewhat increase the absorption in the 450 to 480 nm waveband relative to other parts of the spectrum. In the dinofla-gellate Glenodinium, the increase in concentration of the peridinin/chloro-phyll a-protein associated with growth at low irradiance causes absorption to rise more in the 500 to 550 nm region than elsewhere in the spectrum.1083 These comparatively subtle changes in the shape of the

Phycocyanin Absorptio 550

Fig. 12.15 Absorption spectrum of blue-green algae as influenced by spectral quality of light field during growth (after Bennett and Bogorad, 1973). Cultures of Calothrix 7601 (formerly Fremyella diplosiphon) were grown in red light or in fluorescent light (enriched in the green-yellow waveband), and the absorbance spectra of the whole cells were determined on suspensions containing 0.68 mgdry mass ml"1. The presence of high levels of phycoery-

thrin (PE) in the fluorescent-light-grown cells (____ ) and of phycocyanin

(PC) in the red-light-grown cells (----- ) is apparent from the spectra.

Fig. 12.15 Absorption spectrum of blue-green algae as influenced by spectral quality of light field during growth (after Bennett and Bogorad, 1973). Cultures of Calothrix 7601 (formerly Fremyella diplosiphon) were grown in red light or in fluorescent light (enriched in the green-yellow waveband), and the absorbance spectra of the whole cells were determined on suspensions containing 0.68 mgdry mass ml"1. The presence of high levels of phycoery-

thrin (PE) in the fluorescent-light-grown cells (____ ) and of phycocyanin

(PC) in the red-light-grown cells (----- ) is apparent from the spectra.

absorption spectrum will indeed have the effect of matching the absorption spectrum of the cells better to the spectral distribution of the blue-green light field that prevails at increased depth in many marine waters and so can legitimately be regarded as examples of ecologically useful chromatic adaptation. Nevertheless, the effects of such changes are quantitatively less important for total light capture than the increase in absorption throughout the spectrum resulting from the general increase in pigment concentration. For clear-cut instances of chromatic adaptation we must turn to the biliprotein-containing groups, the Cyanophyta and Rhodophyta.

The changes in the levels of phycoerythrin and phycocyanin in blue-green algae in response to growth in light of differing spectral quality are such as to lead to drastic alterations in the absorption spectra. As shown in Fig. 12.15, the phycocyanin-dominated cells absorb much more strongly in the 600 to 650 nm region than the phycoerythrin-dominated cells, which in turn absorb more strongly in the 500 to 575 nm region. There is no doubt that the former cells would be better equipped to collect light from an underwater light field of an orange-red character, while the latter cells would harvest more photons from a greenish light field. Underwater light fields with a predominantly orange-red character would almost never be found in marine systems, but do exist in inland waters strongly coloured by soluble and particulate humic materials (see Fig. 6.4d). Green light fields are, of course, common in natural waters. Thus, light climates to which these two kinds of cell would be well matched do occur in aquatic ecosystems, but there is a lack of field data on the extent to which adaptation of this type actually happens in nature.

The ratio of biliprotein to chlorophyll can also, as we have seen, change in accordance with the prevailing light. As light intensity diminishes, even when the spectral composition is unaltered, the biliprotein/chlorophyll ratio increases to an extent varying from one blue-green- or red algal species to another. Since this change can be brought about by variation in intensity alone, it could be argued that this is simply 'intensity adaptation' and is not true chromatic adaptation since it does not require a change in spectral composition to bring it about. On the other hand, diminution of light intensity in the underwater environment, as opposed to the laboratory, is most commonly associated with increase in depth in which case it is associated with a change in spectral quality, in particular with a removal of red light. In the course of evolution, therefore, the common association between low irradiance and the virtual absence of red light might well lead to the development of regulatory mechanisms that respond automatically to lowered intensity by increasing the synthesis of pigments, such as phycoerythrin, which absorb in spectral regions other than the red waveband. The plant does not necessarily have to possess a chromatically specific detection system in order to undergo chromatic adaptation. The increase in biliprotein/chlorophyll ratio as light intensity diminishes might reasonably be regarded as both intensity and chromatic adaptation: while it is triggered off by falling intensity, at the same time it makes the cells chromatically better adapted to the particular spectral character that dim underwater light fields usually have.

Little information is presently available on the extent to which this kind of adaptation is of ecological significance. Limited field studies indicating an increase in biliprotein/chlorophyll ratio with depth have been carried out on two red algal species (§12.4).

The non-complementary kind of chromatic adaptation that occurs at relatively high light intensities in red algae, in which the adaptation seems to be directed towards achieving a balanced excitation of the two photosystems (§12.3) is accompanied by substantial changes in the absorption spectrum (Fig. 12.8). This kind of adaptation has not yet been described in the field. It is most likely to be found among algae growing at relatively shallow depths. On the basis of the laboratory studies and theoretical explanations169,806,1490 one might predict that with increasing depth and therefore increasing green/red ratio in the underwater light, the phycoerythrin/chlorophyll ratio would at first decrease to ensure equal excitation of the photosystems and then increase again as the need to capture all available quanta became paramount. Although this has not yet been described for a red alga, what could be an analogous phenomenon has been reported for a brown alga. As we noted earlier, in Dictyota dichotoma at a Spanish coastal site, the fucoxanthin/chlorophyll ratio decreased by 42% between 0 and 10 m depth, and then increased again to its original value between 10 and 20 m depth. If, as is likely to be the case, fucoxanthin transfers its excitation energy primarily to photosystem II, then the increasingly blue-green character of the light with increasing depth might lead to greater excitation of photosystem II than photosystem I, and a decrease in the fucoxanthin/chlorophyll ratio could rectify this. At greater depths still, the need to harvest all available quanta becomes of dominating importance and so the fucoxanthin content is increased again.

In the more densely vegetated parts of the aquatic environment, the ability to compete with other plants for light and/or to tolerate shading by other plants is of great importance. On a priori grounds it seems likely that plants that find themselves in dim light, not because of great depth but because of overshadowing by other plants, will undergo similar kinds of shade adaptation to those associated with increased depth, but the topic has received little experimental attention in the case of aquatic ecosystems. An example of shade tolerance enabling a plant to withstand competition for light is the previously mentioned increase in phycoerythrin content in Chondrus crispus plants overgrown by epiphytic diatoms.1122

A special case of shade adaptation is that of the microalgae living in and under the annual sea ice in North and South polar marine environments. In the Antarctic pack-ice these algae are present at a concentration in the region of 100mgchl a m~2, and since the area covered by the annual expansion and contraction of the ice is about 15 million km2, and the algae are released into the water during the summer thaw, it seems likely that these ice algae make a substantial contribution to the productivity of the polar marine ecosystem.186,1376 The sea-ice algal community is dominated by pennate diatoms, and its photosynthesis saturates at low incident irradiance values, indicating a high level of shade adaptation.258,1033,1137 While there is some indication of a modest capacity for ontogenetic shade adaptation within this community,261,1033 it appears likely that the shade adaptation it exhibits is mainly phylogenetic in nature, i.e. the species present are likely to be genetically adapted to low irradiance.258

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