Schweiz. Z. Hydrol. 49/2, 1987
0036-7842/87/020220-1751.50 + 0.20/0 ~.Q 1987 Birkh/iuser Verlag, Basel
The response of phytoplankton communities to changing lake environments Presented at the International Conference on Lake Restoration in Zfirich, 3-4 November 1986 By Colin S. Reynolds Freshwater Biological Association Windermere Laboratory
ABSTRACT In this paper, empirical relationships between the mean phytoplankton biomass and limiting nutrient availability and between the underwater extinction of light and the biomass are used to define some of the physical aspects of lake environments subject to cultural eutrophication or to corrective restoration measures. The distinctive floristic distributions of different algae among such environments are shown to be closely related to general morphological and physiological properties of the algae themselves and that species sharing similar size- and shape-adaptations also share similar ecological growth and survival strategies. From the~ general predictions of the responses of phytoplankton to changing lake environments, it is deduced that deep lakes are slower to respond than shallow ones but that the transition between nutrient- and light-limitation is relatively abrupt: "resilience' of the system to restoration measures may be an expression of their progress towards the transition.
1. Introduction
The diagnosis of the causes and consequences of lake eutrophication, together with the essential rationale underpinning the corrective measures applied in restoration techniques, have proved deceptively simple. Simple, because the average standing crops of planktonic algae maintained in the open waters of a majority of lakes are directly related to the availability of a limiting nutrient which, in many instances, is phosphorus. This relationship has been progressively refined, culminating in such elegant regression models as those of Vollenweider [52] and Lee, Rast and Jones [18], fitted to appropriate data from a wide range of lakes, corrected to take account of differences in their individual hydrographic and hydrological properties. The literal interpretation is that the greater is the phosphorus loading on to the system, then the greater is the average biomass of phytoplankton maintained in the whole basin. The deceptiveness of the relationship owes to the complexity of the component responses - involving changes in the biochemical functioning of organelles, the physiology of cells, the growth and attrition dynamics of populations of individual species and, eventually, in the composition of the assemblage - to environmental variability generated at scales from a few seconds (e.g. wind-mixing
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through the light gradient) to several years (e.g. interannual variations in nutrient loading). It is particularly remarkable that whole-basin averages of biomass should nevertheless achieve a long-range order of their own [12]. Even so, there must exist extreme effective concentrations of phosphorus, on the one hand, so dilute as to be beyond the ability of phytoplankton cells to accumulate and, on the other, so enriched as to maintain self-shaded populations which no amount of additional nutrient can increase. Thus, the familiar linear representations of the relationship between logarithmic transformations of mean phytoplankton chlorophyll concentration and mean phosphorus availability (fig. la), strictly refer to the rising section of a hyperboloid (fig. lb). Even there, the confidence interval around the model regression is equivalent to + half-an-order of magnitude. This means that 3-fold changes in P-load, either up (continued anthropogenic eutrophication) or down (through deliberate restoration attempts to reduce loadings), need not result in any immediate proportionate change in average biomass yet still conform with the probabilities predicted by the model. This phenomenon is known as "resilience' and is recognized to be more likely to be observed among examples of deeper ( > 40 m) lake systems [47]. An additional complication is that the species composition of the phytoplankton may alter as a consequence of nutrient loading rate in a general way [30, 31 ] that is beyond the predictive capacity of the loading models. This is important to the popular perception of lake eutrophication: public concern is much less sensitive to increases in biomass per se than to the enhanced production of species (such as bloom-forming cyanobacteria) which sully the appearance of lakes, interfere with recreational activities, threaten existing food chains or the survival of prized fish species and render more difficult the treatment of a potable water supply. An improved understanding of the factors involved in compositional changes is desirable from the point of view of defining 'tolerable' nutrient loads, of
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predicting the effectiveness of reduction measures and of devising reliable alternative techniques of lake restoration. The present paper seeks to address the general mechanisms and responses contributing to alterations in the species-structure of limnetic phytoplankton, consequent upon altered nutrient loadings. The approach is mainly discursive invoking some of the recent progress towards the recognition of discrete functional associations of phytoplankton species and of the environmental factors regulating their selection, development and resultant distributions, in time and in space. These aspects of phytoplankton ecology have been discerned from numerous observations on natural assemblages and have been supported by the results of experiments carried out in the laboratory and in model lake systems. By relating the dimension of phosphorus availability to the impact on the underwater light field made by the supportable biomass, the selective bias is shown to be theoretically predictable.
2. Phytoplankton associations and environmental selectivity The species assemblages comprising the phytoplankton in given lakes and at given points in time are infinitely diverse. As examples of this diversity, it is sufficient to distinguish among planktonic flora of sewage oxidation ponds (perhaps dominated by such genera as Chlorella, Scenedeamus, Ankistrodesmus, and Euglena), of mesotrophic temperate lakes in spring (Asterionella, Cyclotella, Melosira spp.), of eutrophic lakes at the time of their summer maxima (Ceratium. Peridinium, Microcystis), of shallow exposed basins (prone to dominance by Oscillatoria spp.) and of small oligotrophic waters, supporting populations of Chrysophyceae (like Dinobryon and Uroglena) together with colonial chlorophytes ( Sphaeroc;vstis, Gemellicvstis ) and various desmids ( Staurastrum, Cosmarium ) . Relating these distributions of algae to critical environmental variables has provided one of the most enduring problems in phytoplankton ecology [6, 14, 26, 27, 45] and it has been subject to a variety of observational and experimental approaches [22-25, 44, 51]. Revealing though these various studies have been, there is still no universally accepted theory to explain why certain species should be abundant in particular lakes at particular times or why they should be replaced by others at different stages in the development of the lake systems in question. The approach to these problems that my own studies have followed has been aimed at defining supra-specific functional groupings of species ('associations') and determining gross variations in the environments that select for or against characters common to those functional groups. This is not merely an expedient way of ignoring the real interspecific differences among the precise environmental optima that have been shown to exist but is a way of classifying and defining observable phenomena of compositional changes for the purpose of establishing patterns. Moreover, it is an approach modelled on the historical development of terrestrial plant ecology, yet is one which permits much of the published information of the biology of individual plankton species to be more readily assimilated [33]. It is also an approach that has comprised several component facets. The first of these, the delimitation of species associations, was based on a phytosociological analysis [1] of several hundreds of individual phytoplankton samples collected from a selection of
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contrasted lake systems at different times of the year, each being treated as a sociological relev6. This permitted a preliminary grouping of individual species which frequently occurred simultaneously, whose waxing and waning were similarly phased and which represented mutually alternative dominants of the phases concerned [32]. With subsequent expansion and refinement [34], taking account of a wider range of lakes and their planktonic assemblages, the list of such discrete species-associations currently numbers some 20 categories (table). Using the alphanumeric labels ascribed to each association, their representation could be consistently described on the basis of their seasonal occurrence in lakes of differing morphometries and trophic status. For example, the sequences in mesotrophic lakes were shown to approximate to B - - , E - - , F - - , L ~ N while a basic C ~ G ~ H - - , M - - , P pattern was discerned among small eutrophic lakes [34]. More pertinently, many additional sequences from other lakes could be appropriately summarized in the same terms [34, 37]. The next step was to focus on the transitions between consecutive phases of dominance by different associations, in order to gauge the importance of environmental changes. Essentially, two kinds of transition were recognized. One of these represented the smooth replacement of species of one association by those of another, examples of which generally showed consistent, unidirectional patterns (e.g. G to H, H to M, E/F to L but not L to F or M to G or H). Such changes were equated with the outcome of ecological succession, associated with decreasing nutrient availability or the impact of grazing animals [32, 35], consequential upon the ordered development of the plankton community itself. The second category was of changes that were typically abrupt, irregular and without clear directionality. They were recognized to have been consistently induced by major limnological events - such as floods or significantly altered physical stability (especially the onset of thermal stratification or enhanced wind-mixing) - precipitated by sharp changes in the external energy imposed on the system. To differing extents, each event had the effect of resetting the succession back to an earlier stage and either allowing a partial recapitulation of the earlier succession ('reversion') [32] or, if sustained, of initiating an alternative ('shifted') successional pathway. On the basis of these deliberations it was deduced that community processes in phytoplankton are driven by the interaction of two main factor groupings: 1. relative resource stress and 2. the frequency and extent of hydraulic mixing (disturbance factors). This deduction is analogous to recent statements [8, 28, 49] about the structure of other major ecological systems, involving terrestrial animals and plants. It is also relevant to the protracted debate about whether the structure of such ecosystems is governed by equilibrium or non-equilibrium processes (see, for instance [3, 46]). In fact, community organisation is regulated through a 'wobbly compromise' [12] between the two. Essentially, development is autogenic, in response to the activities of and competitive interactions between the organisms present, which progressively modify the environment increase spatial organisation, bring about greater niche diversification and raise the level of biomass supported by the energy and resources available; in the words of Margalef [19], the system 'acquires information'. Allogenic, factors are those imposed externally, simultaneously suppressing spatial structure and integrating (and perhaps enhancing) the resource base. The extent of the disturbance is measured by the amount of 'information" that is destroyed. It has been argued [37] that in most pelagic communities, the inherent instability of the aquatic environment determines that the organisation is dominated by
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small-scale processes and that they are often far from any ecological equilibrium. Indeed, the frequency of intermediate disturbances directly contributes to the maintenance of a large number of co-existing species and the apparent ('paradoxical' [13]) violation of the (equilibrium) principle of competitive exclusion [9]. This hypothesis has been tested against the dynamic responses of individual species present in the natural planktonic assemblages of lakes subject to frequent (10-20 days) episodes of wind mixing and restratification [ ! 1,41] or have been imitated or enhanced by artificially-imposed cycles in limnetic enclosures [42, 43]. A recent paper [37] has reviewed the ranges of several sources of environmental variability (light, nutrients, temperature-induced stability and mixing) that are exemplified among the world's lakes, culminating in the assembly of a series of conceptualized environments bringing together different combinations of limiting nutrient stress and of hydraulic mixing, relative to the vertical attenuation of the underwater light field. In each case, the capacity to support algal growth can be separately represented as being limited either by the light gradient or by the availability of nutrients (fig. 2). In the optimum combination (2a), both light and nutrients are saturating and the response capacity is limited by the maximum rate of net growth that can be maintained; elsewhere, the capacity is regulated by the distribution of resources (working downwards) or by the availability of light (working across). Note that highly-disturbed, resource-deficient environments (2 g) are shown to be untenable habitats [cf. 8]. The conceived dimensions of variability may be further reduced to a single representation of the range of aquatic environments (fig. 3b), which is analogous to of Margalet's [20] summary for the sea (fig. 3a), save that it allows phytoplankton growth to exploit environments that are
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Figure 2. Some possible interrelationships among the depth gradients of light penetration (I), relative mixing (shown by the temperature gradient), and limiting-nutrient concentration (K). The scale of algal growth response to the limiting ~actors is represented by hatching. Note that light availability is usually the key limitation with depth but that this may be further modified by the distribution of nutrients; where b o t h / a n d Kare saturating, the alga's growth capacity alone determines the response (upper part of 2a): redrawn from figure 7 of [37].
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enriched by external loadings and not exclusively by regeneration through increased mixing. Moreover, the direction of autogenic change is shown in the vertical plane; allogenic variations are represented primarily in the horizontal direction.
3. Phytoplankton strategies and community responses The validity of these concepts may be established only by demonstrating that the structure of phytoplankton assemblages respond consistently to the proposed dimensions of environmental variability. In turn, this requirement demands that the adaptive strategies of individual species have evolved differentially to exploit the alternative environments effectively. The present section reviews recent evidence that has been assembled to distinguish among the primary strategies of freshwater phytoplankton. Species best suited to exploit resource-saturated environments are likely to be those which arrive first and reproduce fastest. The major investment is in reproductive rate rather than in the efficient use of available resources. The fastest rates of growth in culture (r > 2 d -~ at 20 ~ under conditions of continuous, saturating light intensities and in near-ideal natural conditions (r > 0.8 d -~) are achieved by small, generally unicellular organisms with intrinsically high surface-area to volume ratios ( > 2.0 lam-~), such as Syneehococcus, Chlorella, Ankyna, Ankistrodesmus spp. [34]. Species advantaged by virtue of their rapid growth rates (r) are said to the 'r-selected' [21], 'velocity-adapted' [48] and, in the terminology of Grimes [8], to have evolved a colonist, 'C-strategy'. Under conditions of nutrient stress, growth rate may fall subject to severe limitation. The selective advantage moves toward species which can nevertheless continue to maintain some growth for longer, either because they sustain it from intracellular nutrient reserves taken up in excess of immediate growth capacity ('luxury uptake') at an earlier stage when
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the nutrient was still readily available ('storage-adapted' species), or because they have an intrinsically-high affinity for the limiting nutrient, as indicated by the gradient of growth rate, r, against the limiting-resource concentration, K. A slow rate of growth may be offset by a restricted rate ofbiomass loss through consumption by planktonic herbivores (for instance, by being relatively larger or otherwise 'unmanageable') or through settling out of the water column (by being suitably motile). Moreover, motility and the ability to self-adjust vertical station potentially permit organisms access to structurally-segregated resources. Species which are able to exploit the theoretical biomass-carrying capacity determined by the limiting nutrient are said to the 'K-selected' [21] or 'stress-tolerant', S-strategists [8]. Planktonic examples include species of Ceratium, Peridinium, Anabaena, Microcystis and Uroglena: all generally occur as relatively large units ('large' cells or large colonial units of cells, > I0 ~~tm3) having low surface area to volume ratios ( < 0.3 grn-') and are strongly motile (velocities > 5 m d -~) but the small surface-area/volume ratios of large units determine that maximal growth rates are relatively slow (generally < 0.4 d-' at 20 ~ are strongly temperature dependent and sensitive to low average light intensities. Accordingly, planktonic S-strategists tend neither to grow well at low temperatures nor in optically-deep well-mixed water columns [38], nor are they likely to dominate the early stages of temporal successions [39]. Different species nevertheless remain powerful competitors under particular combinations of nutrient limitation, especially as some stable equilibrium condition is approached. Hydraulic mixing potentially selects for an alternative suite of strategic adaptations. It should be emphasised that the fastest current velocities generated by light winds (1-3 m s -~) generally exceed the intrinsic rates of movement of planktonic algae (u'), sometimes by several orders of magnitude, and are therefore adequate to entrain and disperse most phytoplankton. Beyond obviating any immediate reliance on swimming movements for maintenance within surface mixed-layers, the intensity of mixing (sensu current velocities) is less critical to suspension than is the absolute vertical extent of the wind-mixed layer (z.,). Loss from suspension follows a hyperbolic decay curve, the exponent of which is -u'/zm. Reduction in the mixed depth (zm decreases) therefore selects against the heavier, non-motile (high-u') algae, if they are unable to compensate the losses through new growth; net increase in diatoms for example, shows a finite dependence on the depth of mixing (generally > 2 m [36]). Motile forms are not necessarily disadvantaged by mixing, provided the mixed layer continues to fulfil the range of their nutrient and energy requirements. However, if mixing extends beyond the euphotic depth (zou;i.e. z~ > z,,), all entrained algae will be subject to a reduction in the average light intensity to which they are exposed, to rapid fluctuations in the instantaneous irradiance received and to spend relatively longer in effective darkness. Accordingly, the selective advantage then passes to those algae which absorb and convert the available photic energy most efficiently, perhaps assisted by light-adaptive responses to low light. Among the morphological and physiological properties of such algae are cell attenuation (which has the effect of increasing the areal projection per unit of photosynthetic pigment), increased chlorophyll content per cell (which raises the photosynthetic capacity per unit of biomass) and increased content of accessory pigments (which widens the available spectrum of usable wavelengths). Examples of algae which are particularly tolerant of high-frequency disturbance in optically-deep mixed layers and which show one or more of these adaptive traits include species of Melosira, Asterionella, Cryptomonas and, especially, Oscillatoria.
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Their filamentous or attenuated shapes attain surface-area-to-volume ratios of 0.3-1.5 I.tm-t in spite of their substantial unit sizes (103-105 lam3) and, under optimum conditions, can nevertheless achieve substantial rates of growth (0.8-1.8 d -~ at 20 ~ So far as deep mixing may be analogized to Grimes' [8] concept of high-frequency disturbance, then these algae may be referred to accordingly as disturbance-tolerant 'ruderals' (R-strategists). It should be noted, however, that within this category, both more opportunistic, fast growing, r-selected species, such as Asterionellaformosa Hass.) and more conservative, slow-growing, temperature-sensitive, K-selected species such as Oscillatoria agardhii Gom. may be discerned. The general effects of environmental selectivity upon the species-structure of algal assemblages may be conveniently summarised by allocating the three basic growth- and survival-strategies to different areas of the triangular representation of the range of aquatic habitats, as shown in figure 3c. Temporal changes in resource stress, along the (vertical) gradient of limiting nutrient concentration, or in disturbance, along the (horizontal) gradient of energy limitation are supposed to select for species of the appropriate primary strategy and, given adequate time for the altered dynamics of growth- and loss-processes to alter the composition of the assemblage, eventually to establish them as its dominants. Reynolds [37] has developed this approach to the problem of relating the species structure of natural mixed populations to critical properties of the environment (or, at least, to those obtaining in the very recent past) by fitting the approximate distributions of the species associations to the same dimensions of variability. This graphical model, redrawn here as figure 4, assumes 1. that all species will attempt to grow whenever and wherever they have the opportunity; 2. that under any given coupling of environmental factors, the species able to maintain the most rapid rate of net increase will dominate, such that species representing primarily C-strategist associations are selected in resource replete environments; but 3. that progressively greater extremes of resource stress or hydraulic disturbance select in favour of associations respectively represented by species whose
Increasing optical depth
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Figure 4. Hypothetical view of the selection of phytoplankton associations determined by optical depth of the mixed layer and phosphorus availability. The extent of tolerance of each grouping is described by the lower right hand corner of the shape but less tolerant associations, represented by species which may grow faster at higher resources and low optical depths and which are more likely to be able to dominate are superimposed. Redrawn from part of figure 8 of [37].
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rates of net increase are relatively more tolerant of nutrient or energy limitation. Although these distributions lack empirical precision, owing principally to a dearth of suitable quantitative data pertaining to specific taxa, Reynolds [37] was nevertheless able to show that the plankton flora in a selection of contrasted lake-types, ranging from nutrient-rich ponds to highly-oligotrophic and to turbid, well-mixed, shallow systems, conformed well to the qualitative model. Moreover, the species-specific responses of the phytoplankton in large limnetic enclosures manipulated with respect to phosphorus loading and to the optical depth of artificially-mixed layers, showed consistently similar results [35, 42, 43]. Far from being disproved, the hypotheses concerning the regulation of species composition of natural phytoplankton assemblages appear to offer a sound base for the explanation and prediction of the responses of planktonic communities to environmental change. 4. Modelling the community responses to eutrophication and lake restoration
Development of such an explanative base clearly requires a level of mathematical quantification which is not currently available. The type of graphical representation that is proposed below (fig. 5) is therefore speculative, oversimplified and entirely provisional. It is nevertheless advanced as an illustration of how compositional responses of phytoplankton communities to long-term environmental changes might be determined and as a stimulus for further studies of the appropriate environmental requirements of individual key species of algae. The axes of the figure are analogous to those of figures 3(b) and 4. The vertical axis is scaled logarithmically in terms of the ambient concentration of biologically-available phosphorus, which might be expressed by its (winter) maximum concentration (sensu Dillon and Rigler [4]) or as an annual net areal P-loading, divided by the depth of the water column through which it is effectively diffused. The model solutions have been generated for each of three arbitrary mixed-column depths (4, 10 and 25 m), without stipulation of whether these should represent the mean depth of the lake of merely that of its summer epilimnion. The horizontal axis is scaled in terms of I*, the mean daily integral of photosynthetically-active radiation (PhAR) to which the phytoplankton, freely circulated through the mixed column, might be exposed. Subject to certain assumptions about the intensity and duration of incident PhA R penetrating the surface of the lake (Io), about the impact of phytoplankton chlorophyll on its subsequent attenuation with depth, and about the phosphorus-dependent concentration of chlorophyll that may be maintained, model solutions of I* against P-availability may be derived for mixed columns of given depth. For the purpose of constructing figure 5, in which appropriate curves for 4-, 10and 25-m mixed layers have been inserted, the following assumptions have been made. 1. Io is set at 32 mol m -2 d-~; this is a reasonable, if notional, estimate of the average daily PhAR-fluence that might be received at the surface of temperate-zone (latitude 50 ~ lakes in summer [37]. 2. Incident light is attenuated with depth, in accord with the Beer-Lambert Law, such that the irradiance (spectral shifts notwithstanding) at any given vertical depth (lz) is given by:
L=Le-~-" where z is the distance beneath the surface and ~ is the vertical extinction coefficient.
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3. The vertical extinction coefficient consists two components: the background absorption contributed by the water, set arbitrarily at 0.2 m -~ (see [17]), and the minimum absorption due to algal chlorophyll. This quantity varies considerably among algae [10, 16, 37] but is here set at 0.01 m 2 (rag chl~) -E. Thus, at a concentration of 1 mg chlo m -3, e = 0.21 m-~; at 100 mg chlo m -3, c = 1.2 m -~. 4. The concentration of chlorophyll a in the water is visualized as a continuous and unvarying function of the phosphorus availability, described by the Dillon/Rigler equation [4], viz. log (chl~) = 1.45 log (P) - 1.14 i.e. chl~ = 0.0724[P] TM 5. The chlorophyll concentration is uniform throughout the depth of the mixed layer. Thus the daily PhAR fluence to the floor of the mixed layer (z = 4, 10 or 25 m) is a direct function of chlorophyl concentration: I n / , = - z(0.01 x 0.0724[P] L~5+ 0.2). In I o. I* is then equivalent to the geometric mean oflz and Io, viz. In 1" = (In/~ + In/o)/2 In this way, the curves generated in the construction of figure 5 describe the expected relationship between I* and [P], so long as the assumptions of the model continue to hold. The differences between the curves at low P availabilities are attributable to the depth differences and the background extinction of the water. As greater concentrations of chlorophyll are supported, I* is further reduced, becoming asymptotic to a phosphorus concentration at which self-shading is total (I* = O). In practice, self-shading is effectively complete when the daily maintenance energy (respiration) is balanced by the PhAR income to the system. From data in the literature, pertaining to studies on light-limited laboratory cultures [7, 10, 15], values of 0.1 to 0.4 mg O2 (mg chl,) -~ h -~, rising to up to 2.0 mg O,_ (mg chl~) -~ h -~ after sustained light saturation. From literature information on the efficiency of chlorophyll-specific photosynthesis against limiting levels of irradiance, collected in [37, 40:6.7-69 mg O: (mg c h l y ~. mol -~ m'], the compensating energies may be calculated to fall in a range 0.03-1.4 tool d -t. These values then determine the upper limit of chlorophyll concentration maintained in the given mixed layers, which higher concentrations of phosphorus can scarcely raise and at which a sort ofequilibrium steady-state is achieved [cf. 53]. It is pertinent to observe that, at this equilibrium, the optical depth of the model mixed layers, scaled in units each equivalent to one halving of I (z~, ./In 2; [e.g. 50]), is approximately constant, within the range 8-20). This quantity is important in the prediction of the likely responses of the phytoplankton biomass to further increases or decreases in phosphorus loading. Also shown in figure 4 is a series of rectangles, representing the approximate environmental limits, in terms of phosphorus and energy requirements, of each of a selection of planktonic algae for which appropriate data exist. The vertical dimension corresponds to the half-saturation coefficient of phosphorus uptake (data from various sources, assembled in [38]). The horizontal dimension is deduced from the extrapolation of observations made on a number of separate populations of the same organisms [38] which define the
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approximate threshold of net light-limited population growth; in order to re-calculate the original data in terms of I*, the relationships between ~, Secchi-disk extinction depth (z~) and daylength derived in [42], have been assumed to apply. Viewed in their entirety, the model [P] vs. I* curves are seen to trace pathways through the rectangles that identify which of the organisms represented might be positively or negatively selected. Clearly, there are many instances where given points on the curves lie within several rectangles simultaneously; in such cases the fastest-growing of the organisms is assumed to be the most advantaged, at least initially. Despite the accumulated shortcoming of the model assumptions, as well as both the paucity of species for which suitable data are available and the arbitrary manner in which they have been applied, the figure nevertheless reasonably portrays several trends in the temporal variability of phytoplankton community composition. For instance, seasonal change in a given lake should take place across a range of mixed depths, through a wide spectrum of I* and within an intra-annual variation in trophogenic-zone P-availability of, perhaps, an order of magnitude: thus hypothetical shifts, from Asterionella-dominance, through Dinobryon to Anabaena and Mierocystis reflect the seasonal periodicity of many temperate mesotrophic or mildly eutrophic lakes [cf. 34]. Acknowledged differences among the plankton tbrms of (say) enriched, turbid shallow lakes (frequently dominated by Oscillatoria), the equilibrium stage of the summer stratification (z < 10 m) in eutrophic lakes, often dominated by Microcystis, and the relative confinement of Eudorina- or Chlorelladominance to enriched, shallow or to the early phases of summer stratification [37] are also crudely represented. In the longer term, the relative increase of Oscillatoria spp. over diatoms and Chrysophyceae in deeper lakes, in response to recent anthropogenic enrichment [26, 29, 54]; or vice versa, in response to corrective reduction in P-loading [2, 5] can be explained against the model provisions. These cases at least suggest that constructions such as figure 5 could be developed and applied to the interpretation and prediction of changes in the plankton flora of lakes in response to environmental changes brought about by incidental eutrophication of lakes or deliberate schemes to bring about the restoration of a former or desired quality. 5. Predicting the responses of phytoplankton communities to altered lake environments
Both the theoretical assessment of the principal driving variables influencing the structure of phytoplankton communities and the preliminary attempt to lend some empirical development of the theory in relation to some specific planktonic taxa provide some insight into the mechanisms of compositional shifts prompted by changing phosphorus loadings. Like the quantitative models of the responses of the ambient phytoplankton biomass to altered P-loadings upon which the present development is based, they lack precision and do not embody a significant time dimension. However, the introduction of biological information at the species level may assist in the understanding of resilience phenomena. In the early stages of enrichment, the major response of the phytoplankton is simply to produce 'more of the same': the 'inoculum effect' [35] ensures that the species already present in the lake have the first opportunity to maintain their share of the total biomass production. This response is well-predicted by the P/chl regressions; for a given increase in areal P-loading, the relative availability of phosphorus is primarily a function of the depth of the lake so affected. Accordingly, the response is more rapid among
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shallower lakes. However, the impact o f increased biomass in the same water column is to increase its mean optical depth and, as indicated in figure 5, to select in favour o f alternative species, more tolerant of the imposed self-shading. According to figure 5, the critical optical depth in this respect occurs in the range 5-10, which is generated by a mean biomass concentration of 65-150 mg chl, m -3 in the 4-m lake and supported by 100-200 mg P m -3 but by < 10 mg chl~ m -3, supported by some 25 mg P m -i, in the 25-m example. in the former case, the enhanced phosphorus loading will already have produced a floristic shift in favour of faster-growing, C-strategist species, but in the deeper lake the shift is essentially from low-nutrient to low-light species. Thus stated, this is the principal floristic response in many instances to eutrophication in larger, deeper temperate lakes. Reduction in the external loading does not produce exactly reciprocal responses. Besides the acknowledged difficulties o f overcoming persistent internal P-loading from reserves accumulated in the sediment, which delays the anticipated depression in the availability of phosphorus, especially in deeper lakes, the advantage of inoculum now lies with undesirable dominants, such as Oscillatoria, and the existing concentrations o f these organisms m a y already be saturated with respect to their phosphorus requirements. N o t only are such species tolerant of enhanced optical depth, but their persistence contributes
20 10
I
E E
10
1 0.1 /~ tool d - 1
0.01
Figure 5. Interrelationships between ambient phosphorus concentration and mean exposure to irradiance (I*) in mixed layers of 4, 10 and 25 m, making certain assumptions about the ambient concentration of chlorophyll supported, the available incident radiation and its attenuation due to mixed-layerchlorophyll (see text); greater P-availabilityand higher coefficientsof verticalattenuation eventually reduce light penetration, increase optical depth and lower the amount of light availableto the population, as traced by the three curves. The paths of the curves traverse rectanglesdelimitedby published values of the given algae, showing where these organisms are likelyto be preferentiallyselected.Original.
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t o its m a i n t e n a n c e . O n l y w h e n t h e i r b i o m a s s is r e s t o r e d t o a s e v e r e l y P - s t r e s s e d c o n d i t i o n will it d e c l i n e s u b s t a n t i a l l y a n d a l l o w t h e m o r e a c c e p t a b l e c h r y s o p h y t e - a n d d i a t o m d o m i n a t e d c o m m u n i t i e s to b e c o m e r e e s t a b l i s h e d . I f e i t h e r t h e n e c e s s i t y f o r , o r t h e s u b s e q u e n t s u c c e s s of, m a j o r l a k e r e s t o r a t i o n s c h e m e s is j u d g e d by t h e c r i t e r i o n o f cyanobacteria-abundance, then not only must greater attention be given to the second a x i s o f t h e t w o - d i m e n s i o n a l m o d e l o u t l i n e h e r e b u t , ideally, t h e a r m o u r y o f r e s t o r a t i o n t e c h n i q u e s s h o u l d b e e x p a n d e d to c o u n t e r t h e o f f e n d i n g o r g a n i s m s b y m o r e d i r e c t m e a n s .
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Address of the author: Freshwater Biological Association, Windermere Laboratory, Ambleside, Cumbria, UK. (GB) LA22 0LP.