The differential ability of aquatic plants to utilise the inorganic carbon supply in fresh waters has been recognised as such for several decades. However, the association of particular types of phytoplankton with particular types of water stretches back almost 100 years, to the days of the Wests and the Pearsalls (West and West, 1909; Pearsall, 1924, 1932) and to the lake classification schemes based on biological metabolism devised by Thienemann (1918) and Naumann (1919). The importance of inorganic nutrients, nitrogen and phosphorus in particular, in governing aquatic metabolism was quickly and correctly appreciated. As the broad correlations detected among indicative types of freshwater phytoplankton and the metabolic state of lakes became developed, particular species or groups of species became classified as indicators of olig-otrophic or of eutrophic conditions (Rodhe, 1948; Rawson, 1956). Many chrysophyte, desmid and certain diatom species were seen to be indicative of oligotrophic, phosphorus-deficient conditions (e.g. Findenegg, 1943). Rodhe (1948) went as far as suggesting that phosphorus levels >20 |gP L-1 may actually have been toxic to chrysophytes. On the other hand, Cyanobacteria, especially those species of Anabaena, Aphanizomenon and Microcys-tis that became abundant as a consequence of anthropogenic eutrophication, were believed to express a preference for high-phosphorus conditions.
Many of these differences can now be explained in terms of the chemistry of carbon rather than of other nutrients. There is no question that the levels of biomass of phytoplankton that may be sustained in a pelagic system are related to the resources available and that the amounts of accessible phosphorus or nitrogen or (in the oceans) iron may well be the biomass-limiting resource (see Chapter 4). Because carbon is unlikely ever to be a capacity-limiting resource and because a large body of literature projects a weight of experimental evidence for species-specific differentials in the uptake capabilities and requirements in respect of (especially) phosphorus and nitrogen, it is understandable that interpretations of species selection in terms of available nutrients should persist (Reynolds, 1998a, 2000a). In fact, the experimental evidence for interspecific differentiation among the dynamics of planktic algae on the basis of their differential abilities to exploit the supplies of carbon has been to hand for many years. Now, detailed biochemical and physiological explanations are available to support the critical role of carbon in distinguishing 'oligotrophic' and 'eutrophic' assemblages.
An indicative anomaly is the example of calcareous (marl) lakes set in karstic, limestone upland areas. Their waters are, by definition, rich in bicarbonate but usually deficient in nitrogen and, partly as a consequence of precipitation as hydroxyapatite (calcium phosphate), phosphorus. The modest phytoplanktic biomass they carry is, however, often dominated by the species of volvocalean green algae, diatoms, dinoflag-ellates and bloom-forming species of Anabaena, Gloeotrichia or other Cyanobacteria, that Rodhe (1948) had associated with nutrient-enriched systems. In describing the sparse phytoplankton of Malham Tarn, situated in the carboniferous limestone formations of northern England, Lund (1961) remarked that it was 'quantitatively typical of an oligotrophic lake but qualitatively representative of a eutrophic one'. In contrast, plank-tic elements most indicative of supposedly olig-otrophic plankton (including diatoms of the genera Cyclotella and Urosolenia, such colonial green algae as Coenochloris, Paulschulzia, Pseudosphaerocys-tis and Oocystis of the O. lacustris group, desmid genera such as Cosmarium, Staurastrum and Stau-rodesmus and chrysophytes that might include species of Chrysosphaerella, Dinobryon, Mallomonas and Uroglena) were conspicuously lacking.
Moss (1972, 1973a, b, c) conducted an important series of experimental investigations of the factors influencing the distributions of algae associated with the eutrophication of erstwhile oligotrophic lakes. He found systematic differences in the dynamic responses of algae to variable pH and/or variable carbon sources to be more striking than those due to variation in the amounts of nutrient supplied (see especially Moss, 1973a), with clear separation between the characteristically eutrophic species that could maintain growth at relatively high pH and low concentrations of free carbon dioxide, and the oligotrophic, 'soft-water' species, which could not. Moss's (1973c) conclusion that the response of natural phytoplankton assemblages to nutrient enrichment ('eutrophication') is not dependent on the principal variant (more or less nutrient) but on the productivity demands on the totality of resources.
Talling's (1976) more detailed experiments on the capacity of freshwater phytoplankton to remove dissolved inorganic carbon from the water established a series (Aulacoseira subarctica ^ Asterionella formosa ^ Fragilaria crotonensis ^
Ceratium hirudinella/Microcystis aeruginosa) of increasing tolerance of CO2 depletion and an increasing capability of staging large population maxima under alkaline, CO2-depleted conditions. The work of Shapiro (1990) confirmed the apparent high carbon affinities of several Cyanobacteria, especially of Anabaena and Micro-cystis, which could maintain slow net growth at pH > 10. That the supply of carbon, rather than any other factor, is limiting under such high-pH conditions is supported by the fact that bubbling with CO2 will restore the growth rate of Microcystis (Qiu and Gao, 2002).
On the other hand, Saxby-Rouen et al. (1998; see also Saxby, 1990; Saxby-Rouen et al., 1996) showed convincingly that the chrysophyte Synura petersenii is unable to use bicarbonate at all and gave strong indications that species of Dinobryon and Mallomonas probably also lack the capability. Ball (in Moroney, 2001) has presented evidence that a number of chrysophyte species, including Synura petersenii and Mallomonas caudata, lack any known kind of carbon-concentrating mechanism. Lehman (1976) had already shown that high phosphorus concentration was no bar to the growth of Dinobryon. Reynolds' (1986b) manipulations of phytoplankton composition in the large limnetic enclosures in Blelham Tarn (see Section 5.5.1), showed that phosphorus was as stimulatory to the growth of chrysophytes (Dinobryon, Mallomonas, Uroglena) as to any other kind of phy-toplankter, provided that the pH did not exceed 8.5. To emphasise the point: neither phosphate nor bicarbonate interferes with the growth of these chrysophytes, so long as they have access to free CO2.
It is now easy to interpret these various findings in the light of understanding about differential abilities to exploit the various available sources of DIC. Eutrophic phytoplankters, including colonial volvocaleans, many Cyanobacteria and several dinoflagellates, are those that tolerate the low free-CO2 conditions of naturally high-alkalinity lakes. The species found in soft waters in which enrichment with nitrogen and phosphorus stimulates greater demands on the DIC reserves may well be selected by their ability to exploit bicarbonate directly and/or to focus carbon supplies on the sites of carboxylation. Olig-
otrophic species have no, or only modest, abilities in this direction. The species of Aulacoseira and Anabaena studied by Talling (1976) are intermediate on this scale. Talling's deduction that the CO2 system in natural waters 'plays a large part in determining the qualitative composition as well as the photosynthetic activity of the freshwater phytoplankton' was prophetic.
Evidence is accumulating to suggest that the carbon dioxide system may be similarly selective in the sea. Normally, upward pH drift in the sea used to be considered unusual. With the exception of Emiliana huxleyi, the formation of whose coccoliths was investigated by Paasche (1964), evidence for the ability of marine phytoplankters to use bicarbonate was still lacking as recently as the mid-1980s (Riebesell and Wolf-Gladrow, 2002). The investigations of Riebesell et al. (1993) confirmed that certain species of marine diatom (Ditylum brightwellii, Thalassiosira punctigera, Rhi-zosolenia alata) appear to depend exclusively on the diffusive flux of dissolved CO2. Growth rates became carbon limited at DIC concentrations below 10-20 |M (0.012-0.024 mg C L-1; pH > 8.1) and stalled completely at <5 |M. The dependence upon diffusive transport and non-catalysed conversion of bicarbonate becomes more problematic among those larger phytoplankters that have a relatively low ratio of surface area to volume, for the flux to the boundary layer and the natural dissociation of bicarbonate is just too slow to compensate the CO2 deficit at the cell surface in the wake of a high photosynthetic demand. In contrast, however, some shelf-water species, such as Skeletonema costatum and Thalassiosira weissflogii, show no growth-rate dependence on free-CO2 concentrations, even at pH levels (>8.5) requiring use of bicarbonate and/or some method of carbon concentration (Burkhardt et al., 1999). Whether carbon dioxide or bicarbonate predominates as the proximal carbon source for the alga is not altogether clear. Bicarbonate may be taken up and converted to carbon dioxide by the action of the enzyme carbonic anhydrase, hydroxyl being excreted to balance the charge, so adding to the prevalence of bicarbonate. Carbonic-anhydrase activity is also detectable on the outer surface of these phytoplankters where the use of bicarbonate is accelerated, especially in response to reducing concentrations of free CO2 (Nimer et al., 1997; Sultemeyer, 1998). However, even the benefits that this ability brings are finite, amounting, in effect, to an acceleration of the reestablishment of the carbonate system (Riebe-sell and Wolf-Gladrow, 2002). Carbonic anhydrase activity is said to reach its peak at CO2 concentrations of ~1 |M, (Elzenga et al., 2000) when dissociation of bicarbonate is likely to yield not more than 10-20% of the carbon flux occurring at the air equilibrium in sea water. Carbon limitation of photosynthetic assimilation and potential growth rate of marine phytoplankton is certainly possible and may occur more frequently in high-production waters than has previously been acknowledged.
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