relationships among the biological properties, distribution, and regulation of production by...

Relationships Among the Biological Properties, Distribution, and Regulation of Production by

Planktonic Cyanobacteria

C.S . REYNOLDS, Freshwater Biological Association, Windermere Laboratory, Ambleside, Cumbria, United Kingdom GB-LA22 OLP

Abstract

Interrelationships between the morphological and physiological properties of selected cyanobacterial species distinguished in the laboratory are used to simulate their population dynamics against realistic scales of environmental variability. Differences in performances are shown to correlate well with the ambient conditions found in the various types of lakes in which cyanobacteria are typically distributed.

INTRODUCTION

Toxic strains of cyanobacteria constitute a major consideration in the assessment of water quality in lakes and reservoirs, whether used primarily for recreational pursuits or as sources of potable supplies. Whereas instances of toxicity to fish, livestock, and human consumers were, at one time, believed to be largely associated with the warmer climates at low latitudes, the application of recently introduced methods of assaying for cyanobacterial toxins (Codd, this volume) testifies to the widespread occurrence of toxic strains among populations in lakes of temperate as well as the tropical and subtropical latitudes. Thus, the potential geographical range of water quality problems presented by toxic cyanobacteria is as broad as the water bodies in which these organisms are able to develop significant populations. The present article addresses the factors that influence the development of large or dominant cyanobacterial populations in lakes, irrespective of whether they prove to be toxic or otherwise. Because the topic has been the subject of recent in-depth reviews (Vincent, 1987; Reynolds, 1987a), much of the present assessment takes the form of a summary of present understanding, although it offers a simulation approach to the appraisal of the problem through the development of comparative time scales to describe the opportunities for the growth of cyanobacteria in lakes and reservoirs. The

Toxicity Assessment: An International Journal Vol. 4, 229-255 (1989) 0 1989 John Wiley & Sons, Inc. CCC 0884-8181/89/030229-27$04.00

consideration begins with some order-of-magnitude approximations of the time scales of growth opportunities available in limnetic systems, as limited by particular physical and chemical constraints that may become operative. Comparable time scales are then proposed that differentiate among the physiological capacities of individual cyanobacterial species to exploit them. On the basis that the respective scales must substantially match if the growth of a given species is to be sustained, the ecological ranges of planktonic cyanobacteria are then reassessed and compared with their known distributions. Finally, the types of water body liable to dominance by toxic strains of given cyanobacteria are discussed.

ENVIRONMENTAL VARIABILITY IN LAKES AND RESERVOIRS

The diversity of limnetic environments among the world’s lakes is extremely wide. The origins and morphometry of basins depend upon geophysical and geomorphological processes in the locations con- cerned. The hydrology and, to a large extent, the hydrography of a lake depend upon relations between basin form and local climatic factors (rate of displacement by inflows, exchanges of solar and kinetic energy from the atmosphere). The latter are closely influenced by location, both with respect to latitude and altitude. The hydrochemistry of lakes is influenced by the age, texture, solubility, and rates of fluvial advection of minerals comprising their catchments, which also condition the patterns of vegetation, land use, and human settlement. The hydrobiology of lake systems is integrated to all these influences through a complexity of adaptive interrelationships, the study of which is encompassed by what is generally understood to be ecology.

In order to rationalize the ecological diversity of lake systems, some preliminary classification of limnetic environments is essential. By far the most successful such schemes have been those based upon their hydrographic characteristics (the periodicity of mixing and stratification of their water columns) and those based upon their capacity to furnish the chemical components required to support life (the “trophic scale”). Implicit in these schemes is the recognition of two major sets of ecological factors: those that govern the availability of essential nutrients (resource factors), and those that tend to displace or disrupt the functional organization of biological systems (disturbance factors). Accordingly, the evolutionary ecology of organisms is dominated by the selection of strategic adaptations directed toward the exploitation of one or other of the primary contingencies provided by the interaction of these factor groups (Grime, 1979): abundant re-

PRODUCTION ECOLOGY OF CYANOBACTERIA/23 1

( C ) ....... ..... ..... ..... .....

...... .....

.......

Fig. 1. Schematic representations of the interaction between resource (e.g., nutrient concentration) and disturbance (e.g., deep mixing) factors in lakes, and its impact on the growth potential (stipple) of planktonic algae. Where light ( I ) and nutrients ( K ) are saturating in the upper part of a stratified column (a), the potential maximum of growth rate is the only control. Increased mixing through a truncated photic layer (b,c) lowers the potential but extends to range beyond the limit of light penetration; lower nutrient lowers the potential (d), and may also remove the site of production to the metalimnion (f). Most lakes fluctuate between the extremes (e). (g) The primary growth strategies of planktonic algae, C (for colonist), D (for disturbance tolerance) and S (for stress tolerance) are selected along the two gradients. (Redrawn from Fig. 14.7 of Reynolds, 1987b.)

sources plus low disturbance favor colonist or fugitive (C-) strategies; tolerance of frequent disturbance in resource-replete environments characterizes “ruderal,” or D-strategists; stressed resources in stable environments favor stress-tolerant (or S-) strategies. The fourth con- tingency (highly disturbed, stressed environments) is generally avoided as being untenable.

In lakes, the primary producing vegetation is dominated by phytoplankton comprising mostly microscopic algae and cyanobacteria adapted to live a pelagic existence suspended in the open water. Collectively, their ecologies exploit much of the spectrum of environmental variability that lakes provide. Reynolds (198713) presented a simple graphic scheme tracing the contingencies between resource and disturbance factors, as perceived at the strictly small-scale generation times of microorganisms. This scheme, shown in Fig. 1, analogizes the distribution of potentially limiting plant nutrients to resource gradients and the frequency of vertical displacement by kinetic mixing

processes to disturbance factors. The capacity of phytoplankton to exploit these contingencies, shown in Fig. 1 by the hatched areas, is limited by one or other of the main factor groups. Again, where both are operative, no part of the water column is available; where neither is limiting, the control lies in the maximum rate of organic growth.

EXPLOITATION TIME SCALES

We may now proceed to define the temporal scales of the opportunities for the growth of planktonic autotrophs. The fundamental scale for this purpose is the generation time of the cell, that is, the period from its formation at one cell division to the time of its own division to form two new daughter cells. Assuming a constant cell mass at division, the generation time ( t ~ ) may be equated with the doubling of the existing cell biomass. Rearranging the logistic equation for the exponential increase of a population No and setting the population (Nt ) after a certain time interval t , at Nt = 2iVo we can solve for t ~ ,

Nt = No ert (1)

where r is the exponential coefficient of growth. Hence

t = ln(Nt/No)/r

t~ = (ln2)/r (2)

Natural cyanobacterial populations dominating open waters of temperate and tropical lakes are typically reported to achi.eve standing-crop levels equivalent to and up to 70 g dry mass m-2 (= 1-2 x 10l2 cells per m-2 of Microcystis aerugznosa). Populations of this magnitude husbanded in controlled limnetic enclosures are known to have origi- nated from inocula of <4 x lo9 cells m-2 recruited from overwintering stocks (Preston et al., 1980); that is, not less than six generations contributed to the eventual maxima. The cumulative time scale of exploitation of the environmental resources necessary to sustain this growth is accommodated within a one- to four-month period (<lo7 s), and is certainly well within the time frame of a calendar year. Both the biomass attained and the exponential rate of increase are key quanti- ties: the first is determined by the capacity of the environment to meet the resources eventually required to sustain its synthesis; the second by the rate at which they can be supplied (resource flux). We must also recognize that conversion of resources into biomass consumes energy (in respiration, excretion) and that biomass is potentially lost through mortality, to consumers and parasites and to physical removal processes (such as “permanent” sedimentation and hydraulic outwash

PRODUCTION ECOLOGY OF CYANOBACTERIA/233

from the lake). In this way, the gross resource requirements are always larger than the simple net sum of the components assembled in the standing biomass.

RESOURCE FACTORS REGULATING CYANOBACTERIAL GROWTH

The purpose of this section is to evaluate the impact of energy and nutrient resources on the generation times of cyanobacteria. For the majority of cyanobacteria, growth is mainly or wholly photoautotro- phic, and thus dependent upon the quantity and quality of the photosynthetically active radiation received, net of the energy con- sumed in respiration. The availability and assimilation of nutrients, which is largely independent of light, may impose a variety of limitations on growth rate at lower population thresholds. For convenience, these may be considered separately.

Light-Dependent Processes

The primary anabolic step in the growth process is the photosynthetic fixation of inorganic carbon into sugars, which can take place only while the cell is positioned in the underwater irradiance field. The photosynthetic apparatus comprises the membranous disk-like thyla- koids, which in the cyanobacteria lie free in the cytoplasm, and the associated photosynthetic pigments. Electrons are stripped from a donor substance (usually H20) and are passed through a series of light-driven transport photosystems to generate the high-energy phosphate bonds used to fix carbon. The photosynthetic capacity (P) of the cell is therefore a function of its ability to intercept available light and yield in terms of fixed carbon:

P = I z a k @ ( 3 )

where Z, is the irradiance at a given depth z beneath the water surface, in mol photons m-2 s-l; k is the surface area projected per unit of photosynthetic pigment, in m2 mg-' of pigment, or per analogue unit of cell mass, for instance, in m2 (mol cell C)-'; @ is the quantum yield of photosynthate per unit of light, in mol C fixed (mol photon)-'; and a is a dimensionless proportionality factor expressing the efficiency of the reaction. The product of these components places an upper limit on the capacity to supply photosynthate for growth, as P (mol C fixed) (mol cell C)-' s-'. Some brief consideration of these components is relevant to the adaptive properties of planktonic cyanobacteria.

234iREYNOLDS

@: The theoretical photochemical requirement to fix one mole of carbon is for 8 mol photons, i.e., @ = 0.125 (mol C ) (mol photon)-'. Among the algae, actual yields for the pigment chlorophyll-a (chl-a) often fall below this level: the deductions by Bannister and Wiedmann (1984) of values within the range 0.08 (kO.01) mol C (mol photon)-' are generally accepted as typical.

k: The chlorophyll-specific projected areas of planktonic algae vary conspicuously within the range of 0.004-0.02 m2 (mg chl-a)-'; 0.01 m2 (mg chl-a)-' is a reasonable approximation (Fig. 2a). Assuming a chlorophyll content of 0.5% of dry cell mass, of which approximately 50% is carbon (Fig. 2b), the equivalent projected area per unit cell carbon may be approximated as 0.01 mg chl-a (mg cell C1-I x 0.01 m2 (mg chl-a)-' x 12000 mg cell C (mol)-' = 1.2 m2 (mol cell C1-l. The product k@ = a is a measure of the carbon-specific photosynthetic efficiency (Fig. 2c): in the present case, a = 0.096 (mol C fixed) (mol cell C)-' (mol photon)-'.

I,: The underwater flux of photosynthetically active radiation (PAR; wavelength 360-750 nm) is related to the surface-incident radiation arriving at the lake surface (la), the fraction that penetrates the surface ( I ; ) , and the exponential gradient of its extinction with increasing depth through the water ( E ) . At a given depth z m beneath the surface, the available light flux is given by

I, = I; e-€* (4) where e is the base of natural logarithms and

The maximum value of IQ is a function of the solar constant, the flux of solar energy upon some notional surface held perpendicular to the sun's rays outside the earth's atmosphere, estimated to be 1350 W m-'. Some 46-48% of this is within the PAR waveband. Passage through even a clear, dry atmosphere usually absorbs >33% of the PAR; hence IQ is always ~ 4 2 5 W mP2. Given 1 mol photon 218 kJ, the sunlight arriving (vertically) at the surface of a tropical lake at the midday zenith rarely exceeds 1.95 mmol photon m2 s-'. Reflectance is least (5-10%) when the sun's rays are perpendicular to the surface, so I ; is generally <1.8 mmol m-2 s-'. Given also a minimum extinction coefficient of 0.1 m-' (approximately the value for pure water averaged across the visible spectrum), it is clear that light is effectively extinguished within the upper 100 m of the lake (Ilo0 -- 0.05 pmol photon m-2 s-'1.

Since IQ decreases with decreasing angle of incidence, its maximum instantaneous value fluctuates both with the hour of the day and


mol C mg chl (mol cell 01: (g cell c i ’ (mol photon) mOl C (mOl Cell C)-’s-’

m2

“Ana

10- O M / c 0.2-

OOSC ag 0 M/c

1.6

0.8 I

temperature, C 2 0.5 lk

4 p

0 4 8 1 2 0.2 0.4 0.6

(h) osc ag

20 20

cn

Fig. 2. Photosynthetic properties of cyanobacteria. (a) The chlorophyll-specific projected areas (k,) of cyanobacterial cells (Ana, Anabaenn circinalis; Aph, Aphanizorne- non flos-aquae; Mic, Microcystis aeruginosa; Osc ag, Oscillatoria agardhii; Osc iso, Oscillatoria agardhii var. isothris; Syn, Synechococcus sp.) and plotted against the product of maximum linear dimension and the surface/volume ratio of the cyanobacterial unit. (b) Variability in the chlorophyll content of cells grown in high (0) and low

average light. (c) The slope of Z-dependent P (= cx) under high- and low-light conditions. (d) A generalized P vs Z plot to show the relative position of 4 . (e) The P plot rescaled to the subsurface attenuation in Z with depth. (f) P vs depth plots a t selected times of the solar day due to diurnal variation in the intensity of surface irradiance (in mmol photon m-2 s-’). (g) Maximum photosynthetic rates of cyanobacteria plotted against temperature. (h) Measured photosynthetic rates of given cyanobacteria when grown under high-light intensities. (i) Ditto, for low-light adapted Oscillatoria and Microcystis cultures. Data from text or from the literature (summarized in Reynolds, 1987a).

236/REYNOLDS

with season, according to the geographical latitude. Reflectance under a clear sky also increases sharply at low angles of incidence, although this is modified by backscattering due to waves and foam lines at the water surface. Moreover, clouds and dust in the atmosphere also significantly reduce photon flux to the lake. Beneath the water surface, absorption and scattering of light by solutes and suspended particles, including planktonic algae, increase the coefficient of vertical attenuation, to reported values in the range of 0.2 to >8 m-'. It quickly becomes apparent that the availability of PAR in a majority of the world's lakes falls substantially below the theoretical optimum. For instance, at realistic values I; = 0.6 mmol photon m-2 5-l and E = 0.6 m-', then the PAR availability at a depth (2) of only 3 m, the residual intensity would be only 0.1 mmol photon m-2 s-'.

The experience of many field and laboratory studies shows that appreciable photosynthetic rates can be maintained at such levels. Taking the proposed typical values for k and a, and assuming a = 1, the carbon-specific photosynthetic rate at 0.1 mmol photon m2 s-l approximates to

1 x x 1.2 m2 (mol cell GI-' = 9.6 x

time taken for the cell to double its carbon content is

= 72.2 x lo3 s = 20h

mol photon m-2 s-' x 0.08 mol C fixed (mol photon)-' mol C fixed (mol cell C-') s-l (6)

Assuming that fixed carbon accumulates exponentially, then the

ln2/ln (1+ 9.6 x

In fact, the rates of photosynthetic carbon fixation by cyanobacteria held in experimental gradients where irradiance significantly exceeds 0.1 m mol photon m-' s-' are not increased in the direct proportion kQ, but rather, reach a plateau level, indicative of light saturation of the maximal photosynthetic capacity (Pmax; see Fig. 2d). The intersect between the initial slope (a) of P on I and the plateau P,, level defines the onset of the light saturation and is referred to as zk. The gross photosynthetic rate of a population of cells ( N ) distributed uniformly through a light gradient is not in direct proportion to the distribution of I (unless I; < I k ) but rather corresponds to the product, N P,, X 0.5 I k (Talling, 1957). The relation translates readily to the photosynthetic productivity of the natural underwater light field (Fig. 2e,f).

P,, is sensitive to temperature as it is, for many species (Fig. lg), some 2.0 to 2.3 times lower at 10 than at 20°C. The light-limited slope of P on I is not necessarily different at lower temperatures but the point of intersection ( I k ) varies with P,,,. The photosynthetic capaci-

PRODUCTION ECOLOGY OF CYANOBACTERIAI23 7

ties of cyanobacteria maintained in cultures under constant conditions of temperature and saturating or near-saturating irradiance levels conform to this basic model, and may be individually characterized in terms of P,,,, its sensitivity to temperature, and the gradient (a ) of light-limited P on I (Fig. 2h). Differences in the photosynthetic behaviors of individual species are related to differences in their typical habits, especially with respect to the size and shape of colonial structures, whereas the high surface area to volume ratios (S/V) of small unicells (e.g., Synechococcus) favor rapid rates of metabolic exchange; the solitary filamentous habit (e.g., of Oscillatoria) projects a greater light-receptive surface per unit mass and so contributes to an enhanced a value.

Cyanobacteria grown at consistently subsaturating light intensities show a considerable physiological adaptability to enhance light absorption. The mechanisms involved include the increase of chlorophyll content per cell (Fig. 2b) and the increase of accessory pigments (such as phycocyanin), which widens the spectral band of wavelengths available. Effectively, these mechanisms serve to steepen the gradient of a (Fig. 2c) and depresszk, so that P,,, is potentially attained at lower levels of irradiance (Fig. 2i). The data of Post et aZ. (1985) illustrate this principle particularly well: the apparent photosynthetic efficien- cies (a) of cultures grown at 20 pmol photon m2 s-’ were 2.5 times greater than those maintained under >60 pmol photon m-’ s-l at the same temperature, owing principally to a fourfold enhancement in the content of C-phycocyanin and a threefold increase in cellular chlorophyll content with respect to high-light material (Fig. 2b,c).

The times taken for cells to photoadapt (i.e., to alter their physiological properties to suit altered photic circumstances) may be equivalent to one or more generation times (Falkowski, 1980; Lewis, Cullen, and Platt, 1984): shorter term physiological responses (min- utes to hours) to change in the perceived underwater light field are always those of an existing set of characteristics “timed” to previous ambient condition (Falkowski, 1984).

Light-Independent Processes

Increase in specific biomass and replication of cell material is equally dependent upon the assembly of components other than photosynthate. The majority of these components are taken up from the surroundings as inorganic solutes and their assimilation into organic structures within the cell can proceed largely independent of light. Steps in this scquence that potentially limit the rate of cell replication involve the absorption of the requisite inorganic substances in appropriate chemi-

238/REYNOLDS

cal form (i.e., both soluble and diffusible), their intracellular transfer to the sites of assembly, and their eventual assimilation into the cellular structure. Maximum assimilation rates are sensitive to temperature (Tamiya et al., 1953) and are often lower than the light- saturated capacity to supply photosynthate; where light is not limiting, in situ growth rates tend to be limited by the intracellular capacity (q ) to furnish the requisite nutrients, as compensated by the uptake of external supplies (V). At steady state (for instance, in a chemostat culture), the rate of nutrient and uptake assimilation (= r ) are approximately balanced. The kinetics of both processes are described by Monod-type equations, which express the nutrient-limited rate as a proportionality of the resource base:

V = V,, . S/ (K, + S ) (7) where V,, is the maximum uptake rate per unit of cell mass, S is the external concentration of nutrient, and K,, the half-saturation coefficient, represents the concentration at which uptake is half the maximal rate.

Uptake raises the intracellular content of the nutrient q , which in turn is assimilated into new biomass. If nutrient limited,

r = rmax . (q - qo)/(K + q - q o ) (8)

where r,,, is the resource-saturated growth rate, qo is the absolute minimum quota as a fraction of cell mass at which no further growth can take place, and K, is the concentration required to sustain half rm,. At the supposed steady state, the nutrient required to sustain r is ultimately met by a commensurate rate of uptake V of nutrient present in the medium at a concentration of S. As the nutrient becomes increasingly scarce, V, q, and hence r are liable to be reduced.

Although many instances of limitation of cyanobacterial growth rates by the availability of nitrogen or other elements have been documented, the nutrient most commonly regarded to regulate phytoplankton production in natural waters is phosphorus. Given that the optimal phosphorus content of healthy, actively growing cyanobacteria is around 1.2% of dry mass, or 9.4 mmol P (mol cell C)-’, the phosphorus requirement for each doubling of biomass is then 0.0094 mol P per mol of carbon assimilated. Taking the earlier worked example of “typical” photosynthetic carbon-fixation capacity 9.6 x

mol C (mol cell C)-’ s-l, the uptake requirement of soluble reactive phosphate to maintin a constant internal P store is equivalent to 0.0902 X mol P (mol cell C1-l 5-l. When compared to experimental determinations of phosphorus uptake rates of P-starved cyanobacteria ( Vmm) introduced into P-replete media, as reported in


I

Osc ag

Ana 11

a

ln I

0.1 1.0 SIV pm-1

9

*OSC ag 6 1 (a) vmax

i 5 4 Ana 11 E - a 2 '1 *Mic

ln 4-J 9 0.1 1.0

SIV pm-1

................................ I ",ax 7

u)

4 - 7

(c) Oscillatoria

a

(d) Microcystis ...........

0.8 1.2 1.6 [PI p m d 1-1

Fig. 3. Nutrient uptake properties of cyanobacteria. (a) Maximum uptake rates of Oscillatoria agardhii, Anabaena flos-aquae, and Microcystis aeruginosa plotted against surfacelvolume ratios of the colonies (b) the half-saturation coefficients of uptake (0, K,) and growth (1, K,; Aph, Aphanizomenon fis-aquae). (c) Reconstructed curve of P uptake vs P concentration for Oscillatoriu agardhii, showing V,,, K , and, r, the level required to saturate growth. (d) Ditto for Microcystis. (From data in the literature, summarized in Reynolds 1987a.)

the literature [0.01-0.8 pmol ' (mg dry mass)-' h-', or 0.068-5.44 x mol P (mol cell C)-' s-'], it is apparent that the growth require-

ment for intracellular P is theoretically sustainable, provided dissolved P is freely available to meet it. It has been suggested (e.g., Sournia, 1 9 8 2 ) that absolute maximal uptake rates per cellhnit are a function of the absorptive surface; thus, the rates per unit of mass might be expected to be related to the surface: volume ratio of the cell or colony. The existence of such a relationship is supported by the plot of the most rapid reported uptake rates for three species of planktonic cyanobacteria against their respective typical surface area: volume ratios in Fig. 3a. The external concentrations of soluble reactive phosphorus required to sustain half the maximal uptake rates of

Oscillatoria agardhii and Microcystis aeruginosa (0.2-0.3 pmol L-'; 6.2-9.3 pg P L-') are plotted in Fig. 3b. Using Eq. (71, the curves describing maximal uptake rate against P concentration are reconstructed for these two species in Fig. 3c,d. The requirement for phosphorus to maintain a constant P : C ratio at the maximal rates of photosynthetic carbon fixation at 20"C, 23.6-35.4 x mol C (mol cell C)-' s-l for Oscillatoria and 36.1-47.2 x mol C (mol cell C)-' s-' for Microcystis (Fig. 2h,i) are respectively inserted in Fig. 3c,d. It is clear that the phosphorus-uptake capacity saturates the growth requirement at external phosphorus concentrations >0.1-1.0 pmol L-'. Uptake in excess of 0.2-0.3 mol P (mol cell C)-' s-' may be used to augment the internal stores (4 ) up to a probable maximum of 2.5% dry mass or 0.02 mol P (mol cell W ' . Internal storage of phosphorus on this scale would still be adequate to sustain two or three cell divisions in a phosphorus-free medium before the cell quota in daughter cells fell to the minimum quota [qo = 0.3-0.4% dry matter; 0.002-0.003 mol P (mol cell C)-'I.

Similar calculations should be made with respect to other nutrients absorbed from the growth medium. For instance, the maintenance of an optimal cellular ratio of N : C (0.14-0.19 molar) at the maximal rate of carbon fixation at 20°C requires the supply of 3.3-6.7 x mol N (mol cell C1-l s-l, or about 15 mol N (mol PI-', 6.5 : 1 by weight. The reported half-saturation coefficients of nitrogen uptake among the cyanobacteria average 3-65 pmol L-', or some 12-15 times those of phosphorus. The ratio between the required external concentrations of nitrogen and phosphorus are reportedly lower among the cyanobacteria than the eukaryotic algae (Smith, 1983; Pick and Lean, 1987) and supposedly contribute to their dominance in particular lakes. Faculta- tive fixation of atmospheric nitrogen among members of the Nostocales (e.g., Anabaena, Aphanizomenon, Cylindrospermopsis, Gloeotrichia spp.) at low external nitrogen concentrations apparently further reduces the N : P ratio of the lake waters in which these species are prevalent, where abundance may be more directly correlated with the concentration of biologically available P (Trimbee and Prepas, 1988). However, dinitrogen fixation represents a significant investment in photosynthetic energy, and also depends upon the supply of iron, molybdenum, and other trace metals in relatively higher concentrations (Rueter and Petersen, 1987).

Respiration

Not all the carbon and other nutrients assimilated are directed towards growth: at the very least, energy is expended in the assembly

PRODUCTION ECOLOGY OF CY ANOBACTERIA/241

E l / " I / /

'D 0v 10 20 30

'a 0.2 0.4

mmd photon m-2 s-l temperature, C 1.61 (c)

06 12 18 06 12 18

1.64

I . . 06 12 18

time of day

Fig. 4. Effects of respiration on cyanobacterial dynamics. (a) Changes in instantaneous respiration rate of Microcystis aeruginosa on transfer to higher light intensity (from data of Ganf, 1980). (b) Dark (basal) respiration rates of cyanobacteria vs temperature (from data summarized by Robarts and Zohary, 1987). (c-D Model recon- structions of photosynthesis (P) and photosynthesis net of respiration (P - R ) under differing die1 time tracks of light intensity ( I ) in mmol'photon rn-'s-'. Original.

and maintenance of biomass, which processes detract from the growth capacity. Moreover, the biochemical pathways of cellular respiration are used to eliminate excess photosynthate from cells when growth is nutrient limited. Much of the species-specific information pertaining to the consumption rates of oxygen in respiration has been determined in darkness and is not necessarily representative of cellular respiration in the light field (Gibson and Smith, 1982; Falkowski, 1984). It is therefore important to distinguish the rates of basic endogenous respiration, corresponding to the metabolism of photosynthate in cell maintenance, from the elevated rates of respiration of excess carbon fixed during the light (Reynolds, 1987a; see also Fig. 4a). Reported

242iREYNOLDS

(basal) respiration rates of light-limited suspensions of Microcystis at 20°C are generally within the range of 9-16 pmol 0 2 (mg chl-a)-' h-' (Ganf, 1974,1980; Robarts and Zohary, 19871, between 1/30 to 1/50 of P,, at the same temperature (Fig. 2g) and about 32-38 pmolO2 (mg chl-al-' h-' (1/20 P,,,) in Oscillatoria ugardhzi suspensions (Jewson, 1976; Jones, 1977; Fig. 4b). In either case, the & l o of respiration is similar to that of photosynthesis (Robarts and Zohary, 1987). Within 10 s of transfer of Microcystis to saturating light intensities, Ganf (1980) observed an accelerated rate of respiration [-25 pmol 0 2 (mg chl-a)-' h-'1 that continued to increase to -50 pmolO2 (mg chl-a) h-', so long as the supersaturating light intensities obtained. The respiration rate decreased to the base level again after colonies were returned to darkness, the time taken for the recovery being dependent upon the length of the period of exposure to saturating irradiances. It should be noted that prolonged exposure to high light levels, especially of cells adapted to low light, also depresses the photosynthetic rate (photoinhibition) and, in extremes, may result in damage to the photosynthetic apparatus.

Assuming such behavior to be typical of cyanobacteria in general, it is possible to calculate theoretical generation times at their maximum rates of cell replication, corrected for respirational consumption of fixed carbon, at given levels of irradiance. For example, Fig. 4c-f traces the model net production (P - R ) in relation to die1 variation in I received by cells held at depths respectively receiving 1/8, 1/4, 1/2, and 1 times the irradiance penetrating the surface of a temperate lake (latitude 50") under clear skies at the summer solstice, assuming no prior adaptation to low light. Under the lowest insolation, wherein photosynthesis is continuously light limited, respiration accounts for the equivalent of 1/40 of P,, through the full 24 h (Fig. 4c). In Fig. 4d, P,, is reached at 08.00, after which R increases to 1/16 Pma. In Fig. 4e,f P,, is achieved earlier in the day but photosynthesis becomes increasingly subject to photoinhibition during the day.

DISTURBANCE FACTORS REGULATING CYANOBACTERIAL GROWTH

Unlike the preceding discussion, which implied a static, near-steady state environment for the growing organism, the present section considers the impact of relatively abrupt displacements in the immediate environmental conditions. Such factors should include physical removal of part of the population (for instance, in the outflow from a lake) as well as removal by biological agents (grazers, parasites,


pathogens). Outwash represents an empirically quantifiable loss of cells that, assuming a uniform distribution, is analogous to dilution, the population decaying at a rate dependent upon the discharge rate from the lake, D m3 s-l, relative to its volume M m3; the potential depletion of a nongrowing population NO after time t is given by

For a net increase in the population, growth must exceed outwash, i.e., when r > (D/M); in highly flushed systems, establishment and survival of cyanobacterial populations may well depend upon the frequency and duration of periods when a high net growth rate ( r ) is sustainable and/or when discharge D is significantly reduced.

Similarly, growth may well be sensitive to the rates of removal by grazing animals. For instance, individual filter-feeding crustacea (e.g., Daphnia) each draws in water from the medium that is passed through the filtration apparatus where food particles, including planktonic algae, are removed before the filtered water is expelled into the medium, at a rate primarily dependent upon the size of the animal and the temperature of the water. The maximal rate of removal of algae j corresponds to the aggregate of the individual filtration rates (3’) of the grazing population present per unit volume of lake water ha):

j = n,F (10) In the absence of growth of the grazed algae, the surviving algal

population becomes progressively diluted through the given unit volume, such that

Nt = No e-jt (11)

By analogy, survival of the population depends upon r > j . It is now well established, however, that the colonial, filamentous, and aggregate-forming cyanobacteria are individually too large to be ingested by Cladocerans, although suitably small ( 4 0 pm) colonies of Mycrocystis, Aphanizomenon flakes, aggregates of Anabaena filaments, and fragmented Oscillatoria trichomes may be removed by filter feeders. Neither are these species typically selected by the herbivorous calanoids that locate and grasp their foods. Certain ciliate and amoeboid protozoans, however, have been observed to feed inten- sively on Anubaenu and Aphanizomenon, and to bring about a sharp reduction in the algal populations (for references, see Reynolds, 1987a). In general, grazing upon other ingestible species of planktonic algae is regarded as having a beneficial effect on cyanobacterial dynamics by reducing competition for resources, including those enhanced by the excretion of nutrients by the animals.

244iREYNOLDS

Vertical Mixing

The inherent variability in the hydrodynamic properties of lakes and the stochastic nature of the fluctuations in their external forcing constitute a potentially major source of disturbance to the environments of phytoplankton. A full exploration of this topic is beyond the scope of the present consideration; this section only attempts to summarize the time and intensity scales of mixing processes, their effects upon the dispersion of cyanobacteria, especially in relation to their intrinsic buoyancy, and the advantages and disadvantages that vertical transport confers to their population dynamics. It is also necessary to distinguish the effects of steady state mixing (i.e., that forced by a constant external input) from those brought about by abrupt fluctuations in the external energy.

Motion in lakes emanates from several sources, including Coriolis’ force (induced by the rotation of the earth) and convection (caused by changes in the relative densities of surface and deeper water, brought about by alternate heating and cooling in the near-surface layers), and is variably augmented by the transfer and dissipation through the water column of momentum induced by wind stress on the lake surface itself. The sizes and configurations of lake basins constrain and modify the patterns of the circulations so generated. Their kinetic energy is dissipated through a “spectrum” of turbulent eddies of diminishing size and velocity. While the driving energy persists, however, water in the smaller eddies is constantly liable to reentrainment in the larger ones.

Turbulent diffusivity is understood to be primarily responsible for maintaining phytoplankton in dispersed suspension (Humphries and Imberger, 1982). The maximum intrinsic settling velocities (W,) of nonmotile planktonic algae (<5 x m s-l) and swimming speeds of motile flagellates (<lop3 m s-l) are insufficient to overcome the vertical down-welling currents (1-2 x m s-l) generated by even light winds (<3 m s-’), which may thus be considered sufficient to maintain them in the near-surface circulation. Many planktonic cyanobacteria are able to regulate their buoyancy state close to isopycny through balancing the cellular content of gas vesicles (gas- filled space) against the ballast of cell components (cytoplasm, stored carbohydrate, protein, and polyphosphate bodies), generally within the range of - 1 x lop5 to + m s-l, although in the case of the largest colonial units (e.g., of Microcystis) the range extends to 3 x m s-’. Under most circumstances, then, the distribution of cyanobacteria within wind-mixed layers is dominated by turbulent diffusion rather than by the buoyancy state of the cells.


The vertical penetration of turbulent mixing is related through the velocities of the major currents and eddies to the external driving energy. Turbulent energy is dissipated through progressively smaller eddies, which are propogated downward either to a depth related directly to the kinetic energy input (Denman and Gargett, 1983) or to the boundary layer adjacent to the lake bottom, whichever is the shallower. Turbulent penetration is resisted, however, by vertical density differences brought about by solar heating at the surface. Where the energy is insufficient to overcome the resistance, turbulence rapidly subsides, with the result that turbulent mixing is confined to a near-surface layer separated from a deeper nonturbulent layer by an abrupt gradient of density and velocity. The location of this gradient represents the base of the mixed layer. Because its position relative to the surface is dependent upon the net balance of heat fluxes into and out of the water, as well as on the intensity of the wind stress, it is also liable to frequent alteration: the mixed layer can contract toward the surface under intense diurnal warming and weakening wind stress, or become enlarged by convectional cooling or increased wind energy at the surface. Indeed, density gradients may form by day and disappear during the night. For this reason, the diurnal mixed layer does not necessarily coincide with the seasonal epilimnion, even though the formation of the latter is due to the balance of analogous interactions integrated over periods of weeks or months (see, for instance, Im- berger, 1985, 1987).

The equilibrium depth ( h b ) to which the water column can be mixed under the influence of a given wind stress and heat flux is instantaneously predicted by the Monin-Obukhou equation,

(12)

where (u*) is the friction velocity of the turbulent motion, QT is the net rate of change in heat storage in the layer, pw is the density of the water, CT is its specific heat capacity, y is the coefficient of its thermal expansion, and g is gravitational acceleration. In fact, changes in the true depth of the mixed layer may lag the Monin-Obukhov prediction by several hours: coincidence obtains only after an appropriate period of constancy of the components in Eq. (12). Nevertheless, the predicted hb value serves as a convenient model solution for the purposes of the present argument, which seeks to quantify the impact of vertical mixing on growth dynamics. Two principal effects may be noted. The first of these is that, a t the scale of cell generation times, the layer may be regarded as isotropic, having unique values for available nutrient resources and (at least) die1 integrals of exposure to PAR. Mixing overcomes one of the two possible environmental constraints upon

hb = 2CT p ~ ( u * ) ~ / ( g y QT)

246/REYNOLDS

nutrient uptake by algae, recognized by Pasciak and Gavis (1974): while not necessarily altering the resource base available within the mixed layer, turbulent transport through the medium maintains the concentration differences between the cell surface and the adjacent fluid, principally by constant renewal of the latter. Extension of the mixed layer also entrains water from a greater depth, which may be richer in nutrients. Against this must be set the fact that vertical transport through the mixed layer exposes cells to rapid variations in the PAR field, which may range between the immediate subsurface irradiance and effective darkness. In order to quantify the effect of these fluctuations upon the growth dynamics of mixed-layer algal populations, it is important to establish empirically both the time taken to transport algae through the mixed-layer light gradient and the relation between the absolute depths of mixing and the gradient to which they will be exposed.

The average time taken (t,) to traverse a mixed layer constrained by a basal density gradient is inversely proportional to the turbulent velocity, ut, which may be shown to be equivalent to half the friction velocity:

t, = h b / &

= hb/(2u*) (13)

A fuller account is given by Denman and Gargett (1983). Here the object is to approximate the time taken to complete one full excursion, up and down through the mixed layer. Suppose a lake located at a latitude of 50" receives full solar radiation at the summer solstice, a total of about 26.7 MJ m-2 over a 16-h day (i.e., a t a daytime mean flux of 464 W m-2). A simultaneous wind blowing continuously at 8 m s-' generates a mean turbulent velocity of 0.01 m s-'. Putting pw = 998.1 kg m-3 at 20°C, (T = 4186 J kg-', and y = 2.5 x K-', Eq. (12) can be solved a t h b = 7.5 m. For comparison, were the wind only 4 m s-', the predicted mixed depth would be -1 m. The mean mixing time in the earlier case is 375 s, or about 12.5 min to make the full circulation. In the l-m layer, the mean mixing time solves at 92 s, or 3.1 min to circulate fully. Now let us assume that of the incoming solar radiation, 0.47 is PAR, so that the daily integral light income to the lake surface is 12.6 MJ m-2 that, ignoring surface reflectance, is supplied at a mean daily flux of 218 W mP2; in conventionally expressed light units (1 mol photon or einstein = 218 kJ), this is equivalent to 1 mmol photon m-2 s-'. As shown in an earlier section, the availability of PAR beneath the surface depends upon the value of the attenuation coefficient E . In very clear water ( E = 0.1 m-'1, the PAR remaining at 7.5 m is given from Eq. (4) as averaging 472 pmol m-2 s-' through the daylight hours:

PRODUCTION ECOLOGY OF CYANOBACTERIA1247

0

C I n u) 1.0

E 0.5

00 08.00 08.30 09.00

..-. -_. _.. --I- il

/*, mol photon m-2 d - l /*, mOl photon m-2 d -1

Fig. 5. Simulations of insolation received by an entrained cell moving through the mixed layer of 7.5 m depth every 12.5 min (see text) between 8.00 and 9.00, when the extinction coefficient E = 0.1 m (a), 1.5 m-' (b), 3.6 m-' (c), and the corresponding tracks (d-0 of photosynthesis (P , continuous line), respiration ( R , fine pecked line) and the difference ( P - R, coarse pecked line); daily integrals of P (continuous line) and R (pecked line) are plotted against daily integral light income ( I* ) assuming a 16-h day, with a total insolation of 57.6 mol photon m-' d-' throughout and varying only E . (g) Simulation for Microcystis. (H) Ditto for Oscillatoria. In addition, the curve for low light adapted Oscillatoria is plotted (coarse pecked line), as is a hypothetical response curve linking the two. Original.

effectively, photosynthetic production of (say) Microcystis or Oscilla- toria colonies, tracking the fluctuations in perceived irradiance (Fig. 5a), would remain light saturated at all depths throughout most of the day (Fig. 5b), despite the frequency of traversing the mixed-layer light

248/REYNOLDS

gradient. Mixing causes no significant change in the modeled growtl rate shown in Fig. 2d. An extinction coefficient of E = 1.0 m-', however, is sufficient to ensure that photosynthesis will be substantially light limited in the lower part of the 7.5-m layer: cells transported through the light gradient now have a high probability of experiencing the full range of light levels every 12.5 min (Fig. 5c). Their photosynthetic and respirational responses are simulated in Fig. 5d. If the instantaneous integral of column photosynthesis corresponds to the product P,,, x (I0 .-0.5 Ik), the time integral (t,) is equivalent to the fraction of each theoretical circulation of the mixed layer (t,) that transported cells pass in the light. With uniform mixing, this is a direct function of the relative depths of the mixed layer (hb) and of the subsurface column wherein net photosynthetic production can be sustained (by analogy to the point where I, = 0.5 Ik). Then,

where

Respiration fluctuates between the basal dark rate and the light- saturated rate.

By extension of this reasoning, the effect of further increasing the extinction coefficient E reduces the opportunity for cells to achieve light saturation of photosynthesis and the populations become increasingly light limited. Putting E = 3.0 m-l yields the simulations shown in Fig. 5e,f. Note that this takes account of the photoadaptation of the light-limited cells, which allows an elevated P,, to be sustained near the surface, albeit very briefly, and permits net photosynthesis to be maintained deeper into the light gradient. In the example shown, t, is just under 2 min in every 12.5 min.

Development Times During Continuous Mixing

While any given combination of extinction coefficient and mixing depth persists, it is possible to construct photosynthetic integrals, corrected for respiration, in order to estimate growth and development times. The simulations in Fig. 5g,h assume a constantly wind-mixed layer, 7.5 m in depth, a constant temperature of 20°C. For convenience, the surface irradiance is also assumed constant throughout a 16-h day at the mean diurnal level of 1 mmol photon m-'s-l = 57.6 mol photon d-'). Then, for different values of the extinction coefficient, I* is


calculated as the logarithmic mean of the irradiance through the layer as a whole from

lnI* = (Inlo + ln17.5)/2 (16) This gives the dimension to the horizontal axis of Fig. 5g,h. The

die1 integral, however, is taken from the aggregate of (14) over the 16-h day as Zt,,

Ct, = h,/7.5 m x 57,600 s (17)

and plotted against I* for the corresponding value of E . The estimated respiration rates are also inserted but calculated over the full day (R x 86,400 s). The simulations in Fig. 5h are for full-light grown Oscilla- toria, using the minimal values from Fig. 2c, and for low-light adapted material, with a hypothetical linking curve supposed to represent the intermediate transition of low-light adaptation. The equivalent data for nonadapted Microcystis are shown in Fig. 5g. According to these plots, the daily growth potential r of Oscillatoria overtakes that of Microcystis at low light intensities, despite the faster light-saturated photosynthetic rate and lower respiration rate of the latter, mainly through possessing a higher (Y value (manifest here by attenuation of the P curve against Z*).

Development Times During Intermittent Mixing: The Role of Buoyancy Regulation

Consideration may also be given to the case when wind mixing is noncontinuous. In fact, diurnal variations in the heat flux across the surface and wind activity are the norm rather than the exception, especially at low latitudes (Imberger, 19851, although they are rarely as abrupt as the transition simulated in Fig. 6, in which the following assumptions have been made: A wind that has for several days continuously mixed the surface waters of a lake to a steady depth of 7.5 m instantaneously abates and the entire column becomes immediately static. The incident light entering water and its vertical extinction are unchanged through this transition and for a further 16 h thereafter, at 1 mmol photon m-2 s-l and E = 1.0 m-', respectively however, the water temperature does not alter with depth or in time, but remains at 20°C throughout the erstwhile mixed depth, and until the instant of transition, both Oscillatoria (Fig. 6a) and Microcystis (Fig. 6b) are fully entrained.

Stagnation of the water column allows the organisms to move vertically under the control of their own buoyancy. During the preceding mixed period, the fully entrained organisms would have

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PRODUCTION ECOLOGY OF CYANOBACTERIA1251

been sufficiently light limited (Z* = 23.5 pmol photon m-2 s-’; = 1.354 mol photon m-2 d-l) to have acquired buoyancy; from experimental data collected from the literature (in Reynolds, 1987a) on the difference in density from water of cyanobacteria (p’ - p,) incubated at low light intensities, the OSC~ZZU~OF~U is ascribed a density difference of -27.5 kg m-3 and that of Microcystis (including mucilage) is -2.5 kg m-3. On stagnation of the water column, all colonies immediately begin to float upward at rates determined by the Stokes equation,

-w, = g d 2 (p‘ - pW)/18q . 4 (18)

where - w, is the velocity of flotation, p f - pw is the density difference between the alga and the water, 7 is the viscosity of the water, and 4 is a “coefficient of form resistance” due to nonsphericity of the particle. For spherical Microcystis colonies 250 x lop6 m in diameter (4 = l), the initial flotation rate solves at 85.2 x lop6 m s-l, or 0.3067 m h-’. As cells move into higher light intensities, however, they start to lose buoyancy, with p f - pw decreasing continuously from -2.5 to +5.5 kg mP3 in 7 h (Thomas and Walsby, 19851, i.e., gaining density at a rate of 1.4 kg rnp3 h-l. The process reverses once colonies begin to sink into low light again. Three separate colonies are tracked in Fig. 6b, as their buoyancy is variously lost in saturating light intensities and regained at low light. The net result is that the colonies converge within a relative narrow depth range (2-2.5 m), corresponding to the depth of 0.5 Zk (109 pmol m-2 s-l). In contrast, the initial flotation rates of solitary Oscillatoriu filaments (volume 46,000 ~ m - ~ ; spherical diameter = 44.6 x lop6 m; 4 = 10; see Reynolds, Oliver, and Walsby, 1987) can be solved at 3 x m s-l, or 0.011 m h-’. The vertical position of filaments below the depth of light extinction is thus scarcely altered following the onset of the stagnation period, while the potential reversal of buoyancy (to +22.5 kg m-3 in 24 h; Utkilen, Oliver, and Walsby, 1985) provides for very little sinking during the simulated 16 h of stability (Fig. 6a).

The impact of these movements upon the in situ photosynthetic rates of the organisms is given in Fig. 6c,d. In the case of Oscillatoria, the depth distribution of photosynthetic rates corresponds directly to the light gradient (cf. Fig. 2e), save that significant photoinhibition of the low-light adapted cells is induced in the upper 2 m (>135 pmol m-2 s-l) within 1 h of stagnation. Over the 7.5-m layer as a whole the photosynthetic productivity declines from 16.8 x mol C (mol cell C) s-l to about 5.6 x s-l, this being centered about the depth of I k (3.0 m).

Although there is some photoinhibition of the superficially dispersed Microcystis colonies that reach the surface in the first 3 h after

stagnation, the bulk of the population is able to regulate its buoyancy at subinhibiting irradiance levels, but eventually, well within the photic zone. The contours in Fig. 6d are scaled to the uniformly distributed population, to illustrate the effect of colony convergence to the most productive region of the column (around its Zk, between 1.6 and 2.5 m). This behavior potentially enhances the productivity of the population as a whole, from -10.8 x mol C (mol cell C) 5-l t o about 25 X s-l. The facility of effective buoyancy control in Microcystis is suited both to strongly stratified environments and to rapid recovery of growth in variably mixed columns.

CYANOBACTERIAL GROWTH STRATEGIES AND ENVIRONMENTAL SELECTION

These various empirical data pertaining to the influence of environmental factors upon the population dynamics of cyanobacteria may now be combined to deduce their environmental preferences and limitations. Figure 7 has been devised to represent the abilities of cyanobacteria to exploit environments represented as matrices relat- ing disturbance and resource factors. Figure 7a,b combine gradients of phosphorus concentration against gradients of daily integrals of net photon flux, onto which contours defining the respective generation times of Oscillatoria and Microcystis are superimposed. Both achieve their fastest generation times toward the upper left-hand corner, where resources are optimal and disturbance by mixing is minimal. Only in this region is Microcystis clearly a superior competitor to Oscillatoria. Elsewhere, Oscillatoria growth is better adapted to con- tend with the potential imposition of resource poverty and light limitation through mixing. Indeed, these derivations, based entirely upon the results of laboratory investigations, agree well with knowl- edge of the spatial and temporal locations of dominant cyanobacterial populations. Microcystis is confined to eutrophic lakes that are relatively rich in total phosphorus and is conspicuous during the warmer, high-insolation periods of the year; Oscillatoria spp. tend to dominate rich, exposed, and continuously mixed environments (e.g., the Dutch Polder lakes) and the deep summer epilimnia of larger mesotrophic lakes (Reynolds and Walsby, 1975). Both Microcystis and Oscillatoria tend to be poorer competitors against other algal groups in continuously high-light environments (where small unicellular forms are able to achieve faster growth rates than most cyanobacteria, save Synecho- coccus) and in severely P-deficient oligotrophic waters (Fig. 7c). On the other hand, slower growing larger algae may gain advantage over smaller forms, when the dynamics of the latter may suffer from the


-

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Fig. 7. Contours of net growth in (a) Oscillatoriu and (b) Microcystis in resourceldis- turbance matrices (cf. Fig. l), respectively scaled in terms of phosphorus concentration and the daily perceived light integral Z*; isopleths are generation times tc (in days). (c) Suggested ranges into which various cyanobacterial genera extend; areas occupied by the Sphaerocystis and Chrysophyte associations of Reynolds (1987b) are included. (d) Where there is frequent variability of mixing (horizontal arrows), motile, self-regulating species may be selected; the nutrient-resource base is supposed to influence which genera are preferentially selected in given lakes.

activities of grazing crustacea and/or relatively frequent variability in the relative extent of mixing processes (Fig. 7d). Here, size, combined with motility, is beneficial in advoidance of grazers and in the rapid recovery of an optimal depth distribution with respect to light and nutrient gradients in the wake of a mixing event. Microcystis and other bloom-forming genera appear to be well preadapted in this respect, except in relatively oligotrophic waters or richer habitats where colonial volvocales are able to maintain superior growth rates. Simultaneous limitation of dissolved sources of combined nitrogen of other species may present the nitrogen-fixing members of the Nos-

tocales (e.g., Anabaenu, Aphanizomenon, Cylindrospermopsis, and Gloeotrichia) with a significant ecological advantage over other algae.

To conclude, then, it is apparent that the environmental scales of resource and disturbance limitation upon algal dynamics place very real constraints upon the floristic composition of planktonic communities. Though, by implication, biassed toward the biologies of planktonic cyanobacteria, this account should serve to emphasize that the dominance of cyanobacteria, whether toxic or otherwise, is not inevita- ble. Rather, it is a likely outcome of the appropriate combination of environmental forcing factors acting for a sufficiently long period of time over which appropriate specific preadaptations can be expressed.

References

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Falkowski, P.G. 1980. Light-shade adaptation in marine phytoplankton, P. 99-119. In P.G. Falkowski (ed.), Primary Productivity in the Sea. Plenum, New York.

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Pick, F.R., and D.R.S. Lean. 1987. The role of macronutrients (C, N, P) in controlling cyanobacterial dominance in temperate lakes. New Zeal. J . Marine Freshwater Res.

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