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Figure 5.7

Initial increase in cell populations of Alexandrium tamarense KAC0I in laboratory cultures artificial media with widely differing ratios of N : P: v - I60; - 16; k -I.6. Original data of Dr C. Legrand, replotted with permission. See text for further details.

Oceanography, held in Santa Fe, NM, USA. Her paper was concerned with the development of toxicity in a laboratory strain (KAC01) of the dinoflagellate Alexandrium tamarense in relation to the nitrogen and phosphorus resources supplied. Replicate treatments were grown in artificial media, at 17 ± 1 °C and subject to a 16-h light : 8-h dark cycle, differing only in the concentrations at which nitrogen and phosphorus were supplied. Media contained either 20 |M N and 0.75 |M P (i.e., N : P = 160), or 120 |M N and 7.5 |M (N : P = 16) or 12 |M N and 7.5 |M P (N : P = 1.6). The results, summarised in Fig. 5.7, refer to the increases in cell concentration of algae grown in the three media. They show clearly that initial growth performances in the three media were indistinguishable, though, not surprisingly, they diverged as the experiment progressed. (Note: When Dr Legrand gave her permission to use her data, it was in her full knowledge of the point I wished to illustrate; however, she does not necessarily share my interpretation.)

In nature, phytoplankters inhabit dynamic environments, far removed from the contrived and quasi-steady states of the laboratory, and algal consumption will, in many instances, take one or another of the free resources to below the concentration representing its competitive thresholds. It is within this region of potential growth-rate limitation, that Tilman-type resource-based competition is expected to be strongly expressed. Thus, with external concentrations of (say) MRP falling to below 0.1 | mol P L-1, Asterionella may maintain a rate of replication close to the maximum that the temperature and photoperiod may allow, yet Cyclotella, once its reserves are depleted, is able to maintain only a fraction of its resource-saturated growth rate. Given initial parity, its abundance relative to Asterionella is set to fall quickly behind. As the MRP concentration falls yet further, Cyclotella may cease to increase at all, while Asterionella is still absorbing phosphorus that is now effectively denied to the 'outcompeted' Cyclotella. Very soon, of course, the MRP is too depeleted to be able to support further growth of Asterionella either, and the performance failure is still more abrupt. All this is predicted by the species-specific growth-rate dependence on P concentration (Fig. 5.6).

Against gradients of falling silicon concentration, Cyclotella can continue to absorb silicic acid from concentrations already severely constraining Asterionella. The outcome of interspecific competition betwen other pairs of diatoms may be verifiably predicted according to the model of Tilman et al. (1982). Another, quite separate, illustration of resource competition was described by Spijkerman and Coesel (1996b). Of three species of planktic desmid grown in continuous-flow cultures under stringent P-limiting conditions, one - Cosmarium abbreviatum - showed superior affinity for phosphorus at low concentrations over the other two (Staurastrum pingue, S. chaeto-ceras), even though these have faster maximum P-uptake rates. The outcome of competition in mixed chemostat cultures conformed to the prediction that, at concentrations of <0.02 |imol P L-1, Cosmarium outcompeted the Staurastra but, at higher delivery rates, their faster rates of uptake and growth allowed the Staurastra to dominate the numbers of Cosmarium. If instead of low continuous supply, phosphorus was supplied in single daily doses of 0.7 |imol P L-1, superior uptake rates enabled the Staurastrum species to sequester relatively more of the pulsed resource supply (velocity/storage then proving more advantageous than high affinity).

In none of these cases is the outcome attributable to anything other than the absolute characteristics of the critical resource supply to the needs and sequestration abilities of the organism(s) concerned. In none is the outcome the direct consequence of the ratio of resources available or of the rate at which critical resources are supplied. Thus, at this stage too, it is not the ratio of available resources that determines the outcome. The resource ratio is an interpretative convenience in identifying which of two scarce resources is likely to be, or to become, limiting and it aids the understanding of simultaneous limitation of coexisting species by different resources, provided both are below their respective critical thresholds. When the limiting concentrations of both resources are exceeded, the interspecific competition for those resources is correspondingly diminished, as both satisfy their immediate needs without interference to the other, and the likeihood of the one excluding the other is minimised. The explicit prediction of coexistence, inserted in the top right-hand corner of Fig. 5.6d, is correct but the explanation is different from that applying towards the bottom left-hand side.

There is a further perplexity over the general assumption of resource competition among species, which I have aired at length in certain earlier publications (Reynolds, 1997b, 1998a). From a comparison of the interannual variations in the dynamics and composition of the phytoplankton through successive spring phy-toplankton blooms in Windermere since 1945, several dynamic characteristics have been recognised (Maberly et al., 1994; Reynolds and Irish, 2000). Despite interannual differences in temperature, rainfall and stratification, in the size of the inocula and the rates of growth attained by each of several species of diatom (Asterionella formosa, Aulacoseira subarctica and Cyclotella praeter-

missa), as well as in progressive changes in the nutrient resources in the lake, Asterionella has dominated in all but one of those years. Two trends over the period have been unmistakable. One is that the Asterionella maximum, which, in all years, has been contained ultimately within the capacity of the silicon availability (~30 |imol Si L-1 (Lund, 1950) has, on average, been coming earlier each year (by an average of 30 days over 40 years). Second, during the same period, the MRP available to phytoplankton at the inception of the annual growth increased from ~0.1 to almost 1 |imol P L-1. Early in the period, Asterionella may have seem well suited to the high Si : P conditions, although, in reality, its dominance in any individual year also invoked the size of the inocula and its ability to grow on low daily light doses. By the time of the maximum (and for a substantial period beforehand), MRP levels were below the limit of detection. As the lake has become more enriched with phosphorus, the Asterionella has continued to dominate the early growth stages but it has been able to maintain an accelerating growth rate, all the way to the division that finally reduces the silicon to concentrations limiting its ability to take it up (Reynolds, 1997b). Under these limiting and now relatively low Si : P conditions, should we not expect resource competition to alter the outcome of the spring growth? Reynolds' (1998a) simple model envisaged a typical standing population of Asterionella of 4 x 106 cells L-1 at the time that the silicon concentration is lowered to the point (8 |imol L-1) where its growth rate is increasingly regulated by the rate of silicon uptake. Its next and possibly last doubling (it might take 4-7 days to complete) would require all of the remaining silicon in the water. At the same time, the subdominant Cyclotella, at no more than 0.8 x 106 cells L-1, is experiencing neither phosphorus nor silicon limitation and maintains the maximum growth rate that the temperature and the light regime will allow, as predicted by the Tilman model. The difficulty is that before the altered competitive basis can be expressed at the level of community composition, the silicon is effectively exhausted. There is no advantage to better competitors for a non-existent resource: Asterionella still dominates, despite its (by now) competitive inadequacies.

Table 5.2 Phytoplankters tolerant or indicative of chronically oligotrophic conditions in lakes and the upper mixed layers of tropical oceans

Lakes

Cyanobacteria Chlorophyceae

Chrysophyceae Bacillariophyceae

Synechococcoid picoplankton

Chlorella minutissima, Coenocystis, Coenochloris (Eutetramorus), Sphaerocystis, Oocystis aff. lacustris, Willea wilhelmii, Cosmarium, Staurodesmus Chrysolykos, Dinobryon cylindricum, Mallomonas caudata, Uroglena spp. Aulacoseira alpigena, Cyclotella comensis, C. radiosa, C. glomerata, Urosolenia eriensis

Sources: Pearsall (1932), Findenegg (1943); Reynolds (1984b, 1998a); Hino et al. (1998), Huszar et al. (2003).

Oceans

Cyanobacteria Bacillariophyceae Haptophyta Dinophyta

Prochlorococcus, Synechococcus, Trichodesmium spp. Rhizosolenia, Bacteristrum, Leptocylindrus Emiliana, Gephyrocapsa, Umbellosphaera Amphisolenia, Dinophysis, Histoneis, Ornithocercus spp.

Sources: Riley (1957), Campbell et al. (1994), Karl (1999), Smayda and Reynolds (2001), Karl et al. (2002).

Chronic nutrient deficiencies

There is, however, another way in which resource-based competition shapes communities, at least in oligotrophic waters in which the availability of one or more resources waters is chronically deficient and where species having high uptake affinities for the limiting nutrient(s) are likely to thrive at the expense of inferior competitors. These species are also more likely to provide the inocula in future seasons, so the competitive outcome is magnified from generation to generation. In this way it is relatively easy to hypothesise that the selective traits most favoured in chronically oligotrophic systems - high affinity for limiting nutrients (Sommer, 1984) and small organ-ismic size that is independent of high turbulent diffusivities for their delivery (Wolf-Gladrow and Riebesell, 1997; Section 4.2.1) - select for the relative absence of large species, for the high incidence of nanoplankters (Gorham et al., 1974; Watson and Kalff, 1981) and, especially, picoplankters, both in lakes (Zunino and Diaz, 1996; Agawin et al 2000, Pick 2000) and the open sea (Chisholm et al, 1992; Campbell et al., 1994; Karl, 1999; Karl et al, 2002; Li, 2002). Thus, distinctive groups of species come to characterise severely P-deficient lakes and ultraoligotrophic oceans (see Table 5.2).

It may well be the case that the lakes can be described accurately as having high N : P

ratios. The extent to which the N : P gradient underpins, or even correlates with, compositional patterns in natural lakes has still to be fully resolved. Increasing the phosphorus loads relative to those of nitrogen (thus lowering N : P) does result in compositional shifts, often towards dominance by nitogen-fixing Cyanobacteria, as has been shown in numerous whole-lake fertilisations by Schindler (see, e.g., 1977) and his co-workers. The possible responses to simultaneous enrichment with nitrate or ammonium (raising or maintaining N : P) include frequent incidences of enhanced production of green algae (especially Chlorococcales and Volvocales) but they are frequently confounded by altered carbon dynamics and altered trophic effects attributable to the activities of grazers (Chapter 6). Seasonal changes in resourcing (especially with respect to changing availabilities with depth) may prompt compositional shifts that may be influenced less by ratios than by such mechanisms as highly specialised affinities, alternative sources of nutrients (nitrogen fixation, facultative bacterivory and mixotro-phy) or vertical migration.

The idea that species that are simultaneously limited by different resources do not compete but, rather, coexist successfully has a wide following among plankton ecologists. It conforms to Hardin's (1960) principle of competitive exclusion, which states a long-standing ecological tenet that true competitors cannot coexist. One of its corollaries (that, in a steady state, each truly coexistent species occupies a distinctive niche Petersen 1975) has been advanced to account for the multiple species composition of natural phytoplank-ton species assemblages. The resource-based competition model appears to be powerfully supportive and, provided the limiting conditions persist uninterrupted and for long enough, will lead to the competitive exclusion of all but the fittest species. However, models attempting to verify this provision by simulating rather more than two species competing for more than two limiting resources seem to break down into chaos with unpredictable outcomes (Huisman and Weissing, 2001).

Discontinuous nutrient deficiences

The pattern of change in many pelagic systems is that, as a result of seasonal mixing, storm episodes or periodic inflows, the levels of all nutrients may be raised sufficiently to support the vigorous growth of various species of phytoplankton. The consequence is that the available resources are depleted, one or more to a level that represents a threshold of limitation and the ability of some or all species to grow becomes subject to stress. The initial combination of relative resource-richness and high insolation supports strong growth of many species in the surface mixed layer. Consequential resource depletion tends to proceed from the mixed layer downwards, leading eventually to the progressive uncoupling of resources from light. The water column progressively segregates into an increasingly resource-depleted upper layer and to deeper, increasingly light-deficient layers, wherein available nutrients persist pending exploitation by autotrophs.

Such sequences of events are held to differentiate among the adaptive traits and species-specific performances of phytoplankton, deeply influencing the species selection and seasonal shifts in species dominance. These progressions of composition and dominance are sufficiently striking, in some cases, to have been analo-gised to classical ecological successions in terrestrial plant communities (Tansley, 1939; Reynolds, 1976a; Holligan and Harbour, 1977). The most suc cessful of the early colonist and pioneer species of the pelagic succession have to be poised to invade or to exploit the favourable conditions that open to them. They may ascend to preeminence through an ability to grow faster than their rivals (to 'outperform' them but not to 'outcompete' them). Sooner or later, however, growing demands impinge upon the supply of one or more essential components, after which continued dynamic success requires slightly more specialist adaptations for resource gathering. For instance, noticeably more 'eutrophic species' might start to exclude oligotrophic ones on the basis that the reserve of carbon dioxide is depleted as a consequence of plankton growth. Another possibility is that sufficient growth is accommodated for the light availability in the surface mixed layer to become contested by superior light-harvesters. A third likelihood, to which particular attention is now given, is that algae that are able to penetrate deeper in the water column gain access to nutrients located at depth in the increasingly segregated vertical structure.

The surface mixed layer is an important entity, in limnology as in oceanography. The frequency with which it is turned over (~45 minutes or less: see Section 2.6.5) is much shorter than the generation time of the plankters embedded within the layer. It is quite proper, when considering planktic populations, to regard the surface mixed layer as a single, isotropic environment. In cold or shallow waters exposed to moderate wind stress, the surface mixed layer extends to the bottom of the water column, or to within a millimetre or two of the boundary layer therefrom. Beyond the density gradient separating mixed layer from deeper, denser water masses, many properties of the habitat can differ markedly from those of the surface mixed layer: renewal rate, temperature, insolation, gas and nutrient exchange rates, and so on. Thus, the variability in its vertical extent can also be a critical determinant of performance, alternately entraining and randomising the planktic population through a column of uniform and increasingly low insolation, then disentraining it through stagnating layers. The frequency of the alternation can be critical too: segregation may last for a few hours (as in dielly stratifying systems), a few days (polymictic and atelomictic systems), months on end (seasonal stratification) or more or less continuously (as in meromic-tic systems). The longer is the separation, the greater can be the differentiation with, instead of one, unique environment, a continuous and widening spectrum of individualistic microhabitats (Reynolds, 1992c; Flöder, 1999). Simultaneous feedbacks, including the transfer of settling biomass, cadavers and the faecal pellets of algal consumers to the uninsolated layers below, may further enhance the developing structural discontinuity.

Among the species attempting still to assemble biomass and replicate their numbers, there is a progressive transfer of advantage from those adept at exploiting the mixed-layer resource base (high-sv-1 species, sustaining high replication rates) to those which are equipped to benefit from the separation of the resource base. The situation is reminiscent of the progressive elevation of productive terrestrial foliage from the herb layer to the woodland canopy. In the case of the pelagic, however, it is the downreach of the resource-gathering capacity that is responsible for the functional separation rather than the uplift of the light-harvesting apparatus! The investment by (appropriately adapted) terrestrial plants is in building the mechanical connection. Among the microscopic pelagic plants the adaptive investment is in migration.

Two interrelated sets of adaptations give the advantage to pelagic canopy species. One is the power of motility: if the alga is to have any prospect of covering the vertical distance separating light and nutrient resources, it must be able to determine the direction of its movement. Flagellate genera of the Cryptophyta, the Pyrrhophyta, the Chrysophyta, the Eugleno-phyta and the Chlorophyta would appear to have the essential preadaptations, although the buoyancy-regulating mechanism of gas-vacuolate Cyanobacteria is just as effective a means of propelling migratory movements. The second adaptation, however, is the one that turns the ability to move into the ability to perform substantial vertical migration, i.e. the size-determined capacity to disentrain from residual turbulence (Sections 2.7.1, 2.7.2). Just as small size and maximun form resistance are essential to embedding, so large size and low form resistance are advantageous to ready disentrainment from weakening turbulence and to commencing controlled, directed excursions through the water column.

The velocities achieved can nevertheless seem impressive. Smaller gas-vacuolate, bloom-forming Cyanobacteria (including Microcystis, Gompho-sphaeria, Gloeotrichia, Nodularia, Cylindrospermopsis, raft-forming Aphanizomenon and the species of Anabaena and Anabaenopsis which typically aggregate into secondary tangles of filaments) whose buoyant velocites may reach 40-100 |im s-1 normally sink three to six times more slowly (say 0.6-3.0 m d-1) (Reynolds, 1987a). The movements of large freshwater dinoflagellates like Cer-atium hirundinella and Peridinium gatunense can cover 8-10 m in a single night (Talling, 1971; Pollingher, 1988). The rates quoted for many marine species exceed 100 |m s-1; one or two exceed 500 |m s-1 (Smayda, 2002), although the distances they travel are not given. Volvox undertakes the longest reported circadian migration of any freshwater flagellate, traversing 17 m in either direction of the Cabora Bassa Dam, Mozambique (Sommer and Gliwicz, 1986), at an average velocity scarcely under 1.5 m h-1. In absolute terms, this is modest but, at the scale of the organism, progression at the rate of 1 to 3 colony-diameters per second is impressive.

The question has to be asked whether these migrations do actually yield a harvest of nutrients, sufficient to provide a dynamic advantage over non-migrating species. According to Pollingher (1988), patterns of movement are dominated by a strong, positive phototaxis in the early part of the day (though, generally, their movements will avoid supersaturating light intensities) but they show a decining photo-responsiveness during the course of the solar day. The quality of the light and temperature gradients, the extent of nutrient limitation and the age of the population also influence patterns of movement. The extent of dinoflagellate migrations in a given lake are said to increase with decreasing epilimnetic nutrients, provided the segregated structure persists and the excursions into deeper water provide reward. It is interesting, too, how diminishing nutrient resources should determine that less of the photosynthate produced by buoyancy-regulating Cyanobacteria ends in new cytoplasm and more goes to offsetting buoyancy, forcing organisms to sink lower in the water column (Sas, 1989). Note that shortage of carbon, like shortage of light, means less photosynthate is produced, so organisms become lighter and float closer to the surface. This principle has been demonstrated well in the observations and experiments of Klemer (1976, 1978; Klemer et al., 1982, 1985) and Spencer and King (1985). These self-regulated movements of large plankters certainly seem to open the access to deep-seated nutrient stores. It is apparent, too, that their growth may be enhanced when conditions of near-surface nutrient depletion obtain and the range of vertical migration extends to depths offering replenishment.

There are few studies that provide compelling evidence that this is always the case (Bormans et al., 1999). However, Ganf and Oliver (1982) showed, through observation and careful experimental translocation, that Anabaena filaments picked up substantial amounts of nutrient on their buoyancy-regulated excursions in the Mount Bold Reservoir, South Australia. Raven and Richardson (1984) considered the extra nutrients derived by a migrating marine Ceratium to be only weakly attributable to movement per se (see Section 4.2.1) and much more to the encounters with unexploited nutrients in the (to them) accessible parts of the water column. Deep-water reserves of phosphorus were shown to be within the facultative swimming ranges of Ceratium in Esthwaite Water, UK (Talling, 1971) and within the 'vertical activity ranges' of Ceratium (and, for a time, Microcystis) intercepted by sediment traps in Crose Mere, UK (Reynolds, 1976b).

Thus, strong, self-regulated motility is considered to offer significant advantages, providing opportunities for the selective garnering of the diminishing resources of a structured environment. Adapted species are enabled access to parts of the water column that other algae do not reach, or do not do so sufficiently quickly, or, having done so, cannot reverse their motion to recover a position in the euphotic zone. It should not be assumed that this is the only advantage. The ability to swim strongly and in controlled direction enables an alga to recover vertical station very quickly in the wake of disruptive mixing events, when smaller flagellates or solitary buoyany regulating filaments take hours or days to do so (Reynolds, 1984c, 1989b). Another is that in the face of weak wind- or convective-mixing, the alga can be quite effective in self-regulating its vertical position in order to balance its pho-tosynthetic production and its resource uptake with the rate of cell growth and replication. In this way the cell saves energy in fixing photo-synthate, which, if it could not be made into proteins and new cell material, would otherwise have to be voided from the cell. Organisms which do this very well, such as Microcystis, not only rise to dominance but remain dominant for months (and even years on end) when the appropriate conditions persist (Zohary and Robarts, 1989).

Low insolation and growth-rate regulation

Under conditions of short photoperiods and low aggregate insolation, the problem for phyto-plankton is defined by the point that the alga is no longer able to intercept and harvest sufficient light energy, or to invest it the recruitment of new protoplasm and daughter biomass, at a rate that the temperature and the nutrient supply will allow. Below this level, growth rate is, indeed, light-limited. The curves inserted in Fig. 5.4 differentiate among plankters on the basis of their shape and their capacity for low-light adaptation. The point to notice is that the species that are capable of the fastest rates of growth under relatively high insolation are not necessarily the best adapted to live on small light doses. The limnetic species that do this well include the diatom Asterionella and solitary filamentous species of the Oscillatoriales (Planktothrix agardhii, Limnothrix redekei), in which the capability is correlated with relative morpholgical attenuation (high msv-1: Fig. 5.5). There is often a high capacity for auxillary and accessory pigmentation as well. Thus, their successful contention to perform relatively well in poorly insolated, natural mixed layers owes most to their extraordinary abilities to open the angle of r on I (Fig. 5.4; ar in Fig. 5.5) and, thus, to lower the light intensity at which growth rate can be saturated. In the open, mixed-water column, this extends the actual depth through which growth-saturating photosynthesis may be maintained and, in turn, lengthens the aggregate of probabilistic photope-riod, tp, over that expected for unadapted species in the same water layer. From the least-squares regression fitted to the data in Fig. 5.5, ar = 0.257(msv-1)0

it may be predicted that the stellate colony of Asterionella generates a slope of ar = 0.86 (mol photon)-1 m2, while for a 1-mm thread of Planktothrix agardhii, ar = 1.12. For the small spherical cell of Chlorella, the slope is predicted to be only 0.39 (mol photon)-1 m2. Analogous to the interrelationships among photosynthetic rate and the onset of light saturation of photosynthesis (Eq. 3.5, Section 3.3.1), the lowest light dose that will sustain maximal growth rate at 20 °C is indicated by the quotient, r20/ar. Thus, on the basis of the assembled data (see Table 5.1), we may deduce that Chlorella growth will be saturated by a photon flux of 3.34 mol photons m-2 d-1 (equivalent to a constant ~39 |mol photons m-2 s-1), that of Asterionella by 2.07 mol photons m-2 d-1 (24 |mol photons m-2 s-1), and that of the Planktothrix by 0.77 mol photons m-2 d-1 (9 |mol photons m-2

The inference is emphasised: at irradiance levels exceeding levels of 3.34 mol photons m-2 d-1, Chlorella is the 'fittest' of the three, and its regression-predicted growth rate of 1.84 d-1 outstrips those of Asterionella (1.78 d-1) and Planktothrix (0.86 d-1). However, at light levels equivalent to 0.77 mol photons m-2 d-1, Planktothrix can still be argued to be able to maintain its maximum growth rate (0.86 d-1), and when that of Asterionella is cut back to 0.66 d-1 and Chlorella is severely light-limited at not more than 0.42 d-1. When the low temperatures of high-latitude winters are taken into account, the impact of surface-to-volume relationships modify the relative fitnesses of these organisms. At 5 °C, the predicted resource-saturated growth rates for Chlorella, Asterionella and Planktothrix are, respectively, 0.375, 0.335 and 0.163 d-1 and the respective saturating fluxes are calculated to be 0.96, 0.39 and 0.15 mol photons m-2 d-1. Thus, under an average irradiance (I*) of 0.4 mol photons m-2 d-1 photon flux (equivalent to a constant 5 | mol pho tons m-2 s-1), the light-limited Asterionella might still increase at a rate of 0.335 d-1, which is twice as fast as that of the temperature-limited Planktothrix or the light-limited Chlorella. It is at once appreciable how subtle are the conditions distinguishing among species performances under low doses of light. We might also speculate that although there is an apparent discretion in favour of diatoms in cold, energy-deficient, mixed layers, a little more vigourous mixing (I* falls) or a less severe winter temperature might favour filamentous Cyanobac-teria instead. Reduced mixing and better near-surface insolation immediately favours faster growing nanoplankters such as Chlorella.

Trait interaction and functional differentiation in phytoplankton

The real world of phytoplankton is a blend of deficiencies of differing intensity and frequency, especially with respect to the availability and accessibility of nutrient resources and the solar energy needed to process them. Specialist adaptatations, both in terms of physiological responses at the scale of the life cycle and the traits distinguished at the evolutionary scales, may increase the relative fitness of some species along particular gradients of environmental variability but none is well suited to all conditions. For instance, we may suppose that the most competitive adaptation would be to enable the phytoplankter to self-replicate more rapidly than other species that might be present; hence, a morphology conducive to rapid surface exchanges of nutrients should be favoured, that is, one that maintains a large sv-1. The opposite trend of increasing size (and reducing sv-1) carries advantages of motility, storage and persistence (see also Section 6.7), where the ability to influence vertical position, to gain access to nutrient resources unavailable to other species and to avoid consumption by herbivores offer superior prospects of survival. One advantage has been 'traded' against another, at the price of lowered habitat flexibility: some environments will be better tolerated, or even preferred, by a given species than will others. Such differentiation is, of course, the basis of patterns in the spatial

Figure 5.8

Comparison of growth-rate performances of some phytoplankters. In (a), the minimum light intensity (I) and the minimum soluble-phosphorus concentration ([Slim]) required to saturate the growth at 20 °C of the named algae are plotted against each other. The algae are: Ast, Asterionella; Chlo, Chlorella; Mic, Microcystis; Per, Peridimium cinctum; Pla, Planktothrix agardhii. In the other sub-figures, selected isopleths of growth rate at 20 °C (inserted numerals are x I0-6 s-1) are constructed against the same gradients, for (b) Chlorella, (c) Asterionella and (d) Microcystis. The contours are Redrawn with permission from Reynolds (1997a).

and temporal distribution of species, whereby some are more clearly associated with particular conditions than are others. The further adaptive option for larger algae - that of shape distortion that increases the surface area bounding a given cytovolume - provides not so much a compromise between small and large size but the enhanced ability to process resources into biomass in relatively short periods of exposure to light.

Based upon the growth rates of various species of algae against chosen dimensions in the foregoing sections, we are now able to devise comparative graphical representations of the replicative performances of algae against the two key axes of resource availability and insolation. In Fig. 5.8a, growth-rate contours of several algae are drawn in space defined by light and phosphorus saturation of growth-rate potential. The result is broadly similar to those built on mean underwater light levels and KU values with respect to species-specific phosphorus uptake rates (Reynolds, 1987c) or of light supply and nutrient supply (Huisman and Weissing, 1995). The plots making up the rest of Fig. 5.8 show species-specific replication-rate contours against axes representing steady-state concentrations of phosphorus and the photon flux of white light, at 20 °C. The high levels of resource and light required to saturate the most rapid growth of Chlorella show well against the requirements of four others species (Fig. 5.8a). The sensitivity of Chlorella performance to both light and phosphorus relative to that of Asterionella or of the poorly performing Microcystis against these two criteria is evident (Fig. 5.8b, c, d).

Growth and reproductive strategies When growth under persistently low levels of light and nutrient are considered simultaneously, the basis for some of the very interesting patterns alluded to by Tilman et al. (1982) and by Sterner et al. (1997) may be readily appreciated. Now, for example, we may envisage circumstances under which growth rate in Asterionella is encountering (say) silicon limitation when the growth rate of Cyclotella is constrained by light, and when the growth rate of Planktothrix is too constrained by low temperature or low phosphorus to be able to take full advantage.

There are probably sufficient data to be able to simulate these interactions more rigorously. This is less interesting to pursue than it is to abstract the generalities about the differing adaptations shown by the algae considered here and the broad properties that underpin their strategies for growth and survival. The use of the word 'strategy' in the context of the evolution of life histories is open to criticism on etymological grounds, as it implies that their differention is planned or anticipated in advance (Chapleau et al., 1988). In reality, different patterns for preserving and reproducing genomes have evolved along with the organisms they regulate and, just as certainly, have been shaped by the same forces of natural selection. The patterns are distinctive, separating life histories that, for example, permit opportunistic exploitation of resources and photon energy (as does Chlorella in the example in the previous section) or, alternatively, may provide high adaptability to a low nutrient or to low energy supply (as does Planktothrix). The comparative efficiencies and flexibilities of investment of harvested energy and gathered resources into species-specific biomass define the growth and reproductive strategies of phytoplankton (Sandgren, 1988a).

So far, the discussion has identified three basic sets of strategic adaptations, involving morphologies, growth rates and associated behaviours. The first is the Chlorella type of exploitative or invasive strategy, in which organisms encountering favourable resource and energy fluxes can embark upon the rapid resource processing, biosynthesis and genomic replication (reproduction) that constitute growth. They necessarily have a high growth rate, r, based on an ability to collect and convert resources before other species do and, in this sense (the one followed by most plant ecologists), they are 'good competitors'. Curiously, plankton ecologists reserve this term for the 'winners' of the competition, applying it to those species that specialise in the efficient garnering, conserving and assembling the limiting resource base (K) into as much biomass as it will yield. Thus, the second set of strategic adaptations variously combines high resource affinity and/or specialist mechanisms for obtaining scarce or limit ing resources in short supply with their retention among a high survivorship. Unlike the obli-gately fast-growing, r-selected category, resource-(K-)selected species do not share the constraint of maintaining a high surface-to-volume (sv-1) ratio. However, the acquisitive garnering of diminishing resources sometimes favours significant powers of migratory motility, for which a relatively large size (with attendant penalties in reduced sv-1, slow growth rate and impaired light-absorption efficiency, ea) is essential (see Sections 2.7.1, 3.3.3). Microcystis aeruginosa provides a good example of this second type of strategy that identifies 'winners', or like Aesop's fabled tortoise, the 'good competitor' in the sense understood by most plankton ecologists (Kilham and Kilham, 1980).

The ability to harvest and process energy from low or diminishing irradiances or from truncated opportunities at higher irradiance is favoured by small size or by attenuation of larger sizes (in one or possibly two) planes. These traits represent a high photon affinity, which is not bound exclusively to either r- or K-selection, and to which Reynolds et al. (1983b) applied the term w-selection.

There are clear similarities and apparent analogies in these broad distinctions with the three primary ecological and evolutionary strategies identified among terrestrial plants (Grime, 1977, 1979, 2001). Grime's concept was built around the tenability of habitats according to (i) the resources available and the levels of stress on life cycles that resource shortages might impose on plant survival and (ii) the duration of these conditions, pending their disruption or obliteration by habitat disturbance. Of the four possible permutations of stress and disturbance (Table 5.3), one, the combination of continuous severe stress and high disturbance results in environments hostile to the establishment of plant communities is untenable. These are deserts! The three tenable contingencies are variously populated by plants specialised in either (a) rapid exploitation of the resources available ('competitors' in the original usage of Grime 1977, 1979), which he dubbed 'C-strategists'; or (b) tolerance of resource stress, by efficient matching of the limited supply to managed demand, and

Table 5.3 Basis for evolution of three primary strategies in the evolution of plants, phytoplankton and many other groups of organisms

Habitat duration

Habitat productivity

High

Low

Long

Competitors,

Stress-tolerant

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