Evidence for phylogenetic chromatic adaptation

Changes in the pigment category of aquatic plants with depth are striking in sea water but hard to identify in fresh water, and so we shall here consider marine ecosystems. We shall begin by noting that in all marine waters there is ample light in all wavebands near the surface, and so the theory of chromatic adaptation, which is specifically concerned with light-limited situations, has nothing to tell us about the relative success of the different algal groups in this region: resistance to wave action, for example, or, in the case of upper sublittoral forms, to occasional exposure to the atmosphere, are likely to be more important factors.

While in all waters total irradiance diminishes exponentially with depth, the nature of the change of spectral distribution with depth varies in accordance with the absorption properties of the water. In all waters irradiance in the red waveband diminishes quite rapidly due to absorption by water itself. In very clear colourless waters, attenuation is least in the blue region, and with increasing depth the underwater light becomes first blue-green and then predominantly blue in colour (Fig. 6.4a). In waters with significant amounts of yellow substances there is rapid attenuation in the blue region as well as the red, so that as depth increases the light becomes increasingly confined to the green waveband (Fig. 6.4b). On the basis of chromatic adaptation we might therefore expect somewhat different patterns of algal zonation in the different types of water, and this in fact turns out to be the case.

The depth distribution of the three major eukaryotic algal groups can be expressed in terms of either the biomass, or the number of species, in each group, at a series of depths. Both kinds of information are interesting, the first perhaps more so from our present point of view since it is more directly related to the competitive success through primary production of the different groups: species number, in contrast, can be regarded as a measure of the number of different solutions that the green, brown or red algae have found to the problems of growing at a given depth, or alternatively as a measure of the amount of green, brown or red algal genetic information to be found at that depth. Quantitative distribution data of either type seem to be rather scarce and unfortunately this is especially true in the case of biomass.

We shall first consider waters of the northern hemisphere temperate zone. For the west coast of Sweden (at the entrance to the Baltic Sea), Levring (1959) reported (although quantitative data were not given) that most members of the Chlorophyta occur in the littoral and upper sublittoral zones, the Phaeophyta occur mainly from the littoral zone down to the middle of the sublittoral zone (~15m), and the Rhodophyta occur throughout the euphotic zone but are the predominant algal group in the lower sublittoral zone (15-30 m). Distributions described in other northern hemisphere temperate waters are broadly similar to this but clear-cut zonation appears to be absent. Figure 12.1 shows the variation of species number in the three algal groups with depth at three sites in the British Isles and one from northeastern North America. The numbers of green and brown species decreased with depth. The number of red species at some places increased at first with depth but then began to decrease. At all sites green species were much less common than the other two, and brown species were less numerous than red. At the three sites where green algae were found (Chlorophyta apparently being absent or insignificant at the Scilly Isles site) they penetrated well down into the sublittoral - to about the middle or a bit further - but the brown algae penetrated deeper, and the red algae deeper still. In all cases the red algae dominated the lowest region of the sublittoral. Norton, Hiscock and Kitching (1977) measured the depth distribution of biomass of the more abundant seaweeds on a headland in southwest Ireland, and their data are plotted in Fig. 12.2. Green algae were apparently of no quantitative significance at this site. It can be seen that the brown algae constituted nearly all the underwater biomass throughout most of the sublittoral zone. Brown algal biomass consisted almost entirely of the large kelp Laminaria hyperborea: it reached its peak between about 6 and 10 m depth but decreased sharply below this, falling virtually to zero biomass at 18 m. Below 18m the vegetation consisted mainly of a comparatively sparse cover of red algal species. On a deep-water rock pinnacle in the Gulf of Maine (USA), Vadas and Steneck (1988) observed that kelps (mainly Laminaria sp.) were dominant from 24 m (pinnacle summit) down to 33 m depth. Foliose red algae were present through the kelp zone but extended further: they were dominant at 37 m and reached a maximum depth of 50 m. Crustose red algae became a significant component at about 37 m, and were the dominant algal type in the lowest region, fleshy crusts extending to 55 m and coralline crusts to 63 m depth. Green algae appeared to be absent from the rock pinnacle.

M Wttl Scotland m Haw England, US*

Fig. 12.1 Variation of taxonomic composition of benthic algal flora with depth in northern hemisphere temperate waters. (a)WestofScotland(Argyll and Ayrshire, 56-57 ° N). Derived from data of McAllister et al. (1967). (b) New England, USA (Maine and New Hampshire, 42-43° N). Plotted from data of Mathieson (1979). (c) Isle of Colonsay, Inner Hebrides, Scotland (56° N). Derived from data of Norton et al. (1969). (d) Isles of Scilly, England (50° N). Derived from data of Norton (1968). The curves show the number of red (-•-), brown (—O—) and green (. . .▲. . .) algal species found at each depth. Curves (a), (c) and (d) were derived from the published depth distribution for each algal species.

Depth i mj

Fig. 12.1 Variation of taxonomic composition of benthic algal flora with depth in northern hemisphere temperate waters. (a)WestofScotland(Argyll and Ayrshire, 56-57 ° N). Derived from data of McAllister et al. (1967). (b) New England, USA (Maine and New Hampshire, 42-43° N). Plotted from data of Mathieson (1979). (c) Isle of Colonsay, Inner Hebrides, Scotland (56° N). Derived from data of Norton et al. (1969). (d) Isles of Scilly, England (50° N). Derived from data of Norton (1968). The curves show the number of red (-•-), brown (—O—) and green (. . .▲. . .) algal species found at each depth. Curves (a), (c) and (d) were derived from the published depth distribution for each algal species.

Fig. 12.2 Variation of biomass per unit area of brown and red algae with depth in a northern hemisphere temperate water (Carrigathorna, Lough Ine, southwest Ireland, 51° N). Plotted from data of Norton, Hiscock and Kitch-ing (1977).

Northern European waters contain sufficiently high levels of CDOM to ensure that the underwater light becomes predominantly green in colour,519,636 and the same is likely to be true of the northeastern American coastal waters. In such waters the rate of assimilation achieved by an alga with increasing depth is going to depend on, among other things, how much absorption it has in the green (500-600 nm) band. The green algae, which show relatively low absorption in this spectral region, are the most disadvan-taged, which would explain their small contribution - both in species number and biomass - to the algal community, and the fact that they penetrate least deeply. The brown algae, which show, due to the presence of fucoxanthin, substantial absorption in the 500 to 560 nm region, hold their own through most of the sublittoral euphotic zone. At the lower fringe of the euphotic zone, where the spectral distribution becomes quite narrow, the red algae, whose biliprotein pigments have their absorption peaks within the green region, can compete better for the available light and so come to dominate.

We shall now consider the very different kinds of algal distribution that are observed in coastal waters very low in colour. Taylor (1959) found in

Fig. 12.3 Variation of taxonomic composition of benthic algal flora with depth in a tropical water. Plotted from data of Taylor (1959).

Fig. 12.3 Variation of taxonomic composition of benthic algal flora with depth in a tropical water. Plotted from data of Taylor (1959).

the Caribbean that while red, brown and green species were all well represented in shallow water there was a progressive decrease in species number in all three groups with depth (Fig. 12.3). Proportionately, this decrease was least for the green algae and in the lower 75% of the sublittoral zone there were more green species than either red or brown. Similar distributions have been observed in the Pacific. In Hawaiian coastal waters, green algal species, although overall less numerous, penetrated as deeply as red algal species, and more deeply than the brown.317 In Eniwetok atoll lagoon, Gilmartin (1960) found that although the numbers of green and red algal species were comparable at depths down to 65 m (both greatly exceeding the number of brown species), the greens appeared (on the basis of visual observation) to be dominant in terms of biomass at all stations down to this depth, at which irradiance was 2 to 4% of that at the surface.

Algal distributions in the Mediterranean show some similarities. On a Corsican headland, Molinier (1960) found that green algae penetrated as deeply as 80 m, being replaced below this by red algae. A particularly valuable quantitative study, of the depth distribution of algal biomass on vertical rock faces off Malta, was carried out by Larkum, Drew and Crossett (1967). They measured the dry mass of algal biomass within the three taxonomic groups per unit area of the cliff face, as a function of depth: the results are shown in Fig. 12.4. Down to about 10 m depth

Fig. 12.4 Variation of biomass per unit area of cliff face of green, brown and red algae with depth on vertical rock faces in the Mediterranean Sea (Malta, 36° N). (Plotted from data of Crossett, Drew and Larkum, 1965.)

brown algae were dominant but their contribution to total biomass decreased sharply below this. Green algae became significant at about 15m and were the major component of the community from 20 to 60m (the lowest depth studied). Red algae became significant components only at 30 m and decreased again below 45 m, proportionately as well as in absolute terms.

Littler et al. (1985,1986) used a submersible to carry out a detailed survey of the depth distribution of algae on the San Salvador Seamount, the top of which forms a km2 flat plateau about 80 m below the ocean surface, 6.5 km north of San Salvador Island (Bahamas). The plateau region and the sides of the seamount down to 90 m depth are dominated (% cover) by the brown alga Lobophora variegata, although a wide variety of green, brown and red algae are present. From 90 m down to about 130 m, green and red algae are present but green dominate, the community consisting mainly of four species of the calcareous genus Halimeda, especially H. copiosa. From 130 down to 189 m the assemblage is dominated by a crustose red alga, Peyssonelia, but two frondose chlor-ophyte species are also abundant (at least above 157 m). From 189 down to 268 m the dominant species is a crustose coralline red alga, but upwards of 210 m small amounts of the green alga Ostreobium appear.

It is clear from these various studies that the most significant difference between the colourless and the slightly yellow coastal waters, so far as algal distribution is concerned, is the very much greater success of green algae in the former. This is just what would be expected on the basis of chromatic adaptation. As we have seen, the underwater light field in such waters becomes particularly rich in that blue waveband in which the green algae carry out most of their light harvesting. Except at the greatest depths there is a high proportion of green as well as blue light. Some species of green algae, in virtue of their containing the carotenoid sipho-naxanthin (which when bound to protein in vivo absorbs in the 500-550 nm region), have an enhanced ability to absorb green light. Yokohama et al. (1977) and Yokohama (1981), in a survey of green algal species in Japanese waters, found that in three orders (Ulvales, Clado-phorales and Siphonocladales) siphonaxanthin is present in deep-water species but absent from those growing in shallow water: a plausible example of chromatic adaptation. In certain other orders (Codiales, Derbesiales and Caulerpales) siphonaxanthin is present in all species, even in those from shallow waters: in the latter, Yokohama suggests that siphonaxanthin may be an evolutionary relic, from deep-water ancestors. Among 14 species of the marine Chaetophoraceae (Chlorophyta), O'Kelly (1982) found five with lutein (the most abundant higher plant/ green algal xanthophyll) and no siphonaxanthin, four with siphonax-anthin and no lutein, and five with both. The species having just lutein were found only in the mid- to upper-intertidal habitats, those possessing only siphonaxanthin were confined to the subtidal region, while those containing both pigments occupied intermediate, wide-ranging habitats.

Direct experimental evidence supporting the chromatic adaptation theory has been obtained by Levring (1966, 1968). He measured the photosynthetic rates of samples of green, brown and red algae suspended in bottles at a series of depths in turbid nearshore water (highest trans-mittance in the green) off the Swedish and North Carolina coasts, and in clear oceanic water (transmittance highest in the blue) in the Gulf Stream. To compare the ways in which photosynthesis and irradiance varied with depth he used a parameter, q, which may be regarded as the ratio of the vertical attenuation coefficient for photosynthetic rate to the vertical attenuation coefficient for irradiance. If a particular type of alga becomes increasingly ill-adapted to the spectral distribution of the light with increasing depth, then q will be greater than 1 (i.e. photosynthesis will decrease faster than irradiance); if the alga is better adapted to the spectral distribution found at great depth, then q will be less than 1. Below 10 m, for green algae, q was 1.2 to 1.3 in the turbid/coloured water and ^0.8 in the colourless water, indicating that they were better adapted for photosynthesis at depth in the less-coloured water. In the case of red algae, q was ^0.8 in the turbid/coloured water, indicating improved adaptation with depth, and ~1.0 in the colourless water, indicating little change in adaptation with depth. For the brown alga, Fucus, q was ~1.0 in the coloured/turbid water, but variable (above and below 1.0) in locations with colourless water.

In the case of phytoplankton also there is evidence for phylogenetic i AI n 1 OO ^

chromatic adaptation. , In stratified oligotrophic blue ocean waters, chlorophyll b, which is indicative of the presence of green chlor-ophytes and prochlorophytes, is concentrated near the bottom of the euphotic zone where the light is predominantly blue to blue-green. It is commonly found in these ocean regions that cyanobacteria, such as Synechococcus, occur mainly near the surface, their high levels of the photoprotective carotenoid, zeaxanthin, enabling them to tolerate the intense radiation. Prochlorophytes, such as Prochlorococcus, congregate mainly in the DCM, at the bottom of the euphotic zone, where the Soret band of their divinyl-chlorophyll a enables them to efficiently collect energy from the predominantly blue light field.237,1213,1412,72 In near-surface, nitrate-rich waters, diatoms predominate: their major accessory pigment, fucoxanthin, efficiently harvests the green light that is abundantly present at these lesser depths. Hickman et al. (2009) observed striking vertical gradients in the phytoplankton taxa through the water column across a broad region of the seasonally stratified Celtic Sea. Pigment compositions and the phytoplankton absorption spectra indicated that the different phytoplankton communities were chromatically well adapted to the spectral composition of the light field at the depths where they occurred in the water column. At a mesotrophic and an oligotrophic site in the tropical North Atlantic, Lazzara et al. (1996) found, by comparing the spectral distribution of irradiance (500-530 nm and 470-490 nm, respectively) at the bottom of the euphotic zone, with the peaks in the fluorescence excitation curves, evidence for complementary chromatic adaptation in the phytoplankton community to the prevailing spectral irradiance. In the stratified Sargasso Sea, Bidigare et al. (1990), by comparing the absorption peaks of accessory pigments with the spectral irradiance maxima, found evidence for chromatic adaptation of the phytoplankton.

Pick (1991) studied the distribution of different pigment types of picocyanobacteria in 38 lakes of varying optical and trophic status. Some cyanobacterial picoplankton strains contain only phycocyanin and allophy-cocyanin biliprotein pigments, with absorption peaks at ^620 and 650 nm, respectively, while other strains also contain phycoerythrin, absorbing in the green at ^550 nm. Pick found that as light attenuation among the lakes increased, a trend that would be accompanied by a shift in the underwater spectral distribution from the green towards the red, so the percentage of phycoerythrin-containing picocyanobacteria significantly decreased. In the stratified water of oligotrophic Lake Stechlin (Germany), Gervais et al. (1997) found a deep chlorophyll maximum at a depth of 10 to 15 m, where the prevailing light was confined almost exclusively to the 500 to 600 nm waveband. The DCM was dominated, apart from centric diatoms sediment-ing through from above, by picocyanobacteria containing phycoerythrin, which absorbs strongly at these wavelengths.

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