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Cyanobacterial dominance: The role ofbuoyancy regulation in dynamic lakeenvironmentsColin S. Reynolds a , Rod L. Oliver b & Anthony E. Walsby ca Freshwater Biological Association, Windermere Laboratory,Ambleside, United Kingdom (GB‐), LA22 OLPb Murray‐Darling Freshwater Research Centre, P. O. Box 921,Albury, NSW, Australia, 2640c Department of Botany, University of Bristol, Bristol, UnitedKingdom (GB‐), BS8 1UGPublished online: 30 Mar 2010.

To cite this article: Colin S. Reynolds , Rod L. Oliver & Anthony E. Walsby (1987) Cyanobacterialdominance: The role of buoyancy regulation in dynamic lake environments, New Zealand Journalof Marine and Freshwater Research, 21:3, 379-390, DOI: 10.1080/00288330.1987.9516234

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New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21: 379-3900028-8330/87/2103-0379$2.50/0 © Crown copyright 1987

Cyanobacterial dominance: the role of buoyancy regulationin dynamic lake environments

379

COLIN S. REYNOLDS1

ROD L. OLIVER2

ANTHONY E. WALSBY3

1Freshwater Biological AssociationWindermere Laboratory, AmblesideUnited Kingdom (GB-) LA22 OLP

2Murray-Darling Freshwater Research CentreP. O. Box 921, AlburyNSW, Australia 2640

3Department of BotanyUniversity of Bristol, BristolUnited Kingdom (GB-) BS8 1UG

Abstract The interactions of size, shape, anddensity of cyanobacteria result in a 5-order of mag-nitude difference in flotation or sinking rates which,in turn, influence the extent of their dispersion inturbulent water masses. Active mixing throughresource-replete waters of high clarity favours fast-growing, small-celled species. Where photosyn-thetically active radiation is severely attenuatedthrough the wind-mixed layer, species may rely onturbulent entrainment but must be adapted towardefficient light harvesting (morphological attenua-tion, enhanced pigmentation). In both strongly seg-regated waters (light- and nutrient-rich layersseparated vertically) and waters experiencing high-frequency fluctuations in vertical mixing and opti-cal depth, emphasis is placed on the ability to makerapid, buoyancy-adjusted vertical movements,favoured by large size. The cyanobacterial 1ife-formsrespectively typical of these contrasted limnologi-cal systems — unicellular coccoids (e.g., Synecho-coccus), solitary filaments (e.g., Oscillatoria) andcolonial forms (e.g., Microcystis) — illustrate thediversity of evolutionary adaptations to be dis-cerned among the planktonic cyanobacteria andwhich contributes to their reputation as a promi-nent and successful group of organisms.

Keywords blue-green algae; buoyancy; carbo-hydrate; cell size; colony; cyanobacteria; flotation;gas vacuoles; mixing; phytoplankton; sediment-ation; sinking

Received 19 February 1987; accepted 11 May 1987

INTRODUCTION

The tendency for the plankton of eutrophic lakesto be dominated for considerable lengths of timeby genera of cyanobacteria (blue-green algae, orcyanophyta) is often supposed to be related to theunique biological features of the group as a whole.Their widespread representation in the plankton offreshwaters could depend upon many factors: theirpigmentation, which confers a high photosyntheticefficiency and an ability to sustain net photosyn-thetic production at low photon irradiances; a highlevel of metabolic flexibility, which enables themto tolerate extremes of temperature, alkalinity, andhalinity, as well as to function in micro-aerophil-ous environments; extracellular secretions, whichfacilitate selective ion uptake and which may betoxic to competitors and potential consumers alike;a capacity to store nutrients when present in excessof immediate demand but which sustain growthwhen external supplies are otherwise limiting; thecapacity to fix and assimilate dissolved nitrogen gaswhen the external concentrations of dissolvednitrate and ammonia fall to low levels, often witha concomitant reduction in the ratio of availabil-ities of N : P; and an ability to regulate the buoy-ancy imparted by the presence of intracellular gas-filled spaces, the gas vacuoles. It is not so muchthat individual cyanobacteria are adapted to a fullrange of environmental variability which accountsfor the ecological success of the group, as that par-ticular species are each adapted to selectivelyexploiting different parts of the wide spectrum ofenvironmental circumstances that may be gener-ated in lakes. We will demonstrate that interactionsamong buoyancy and its physiological control, thesize, hydrodynamic shape, and the resourcerequirements of individual cyanobacterial speciesare of profound importance in determining selec-tion under given limnological conditions.

This short overview proceeds from a consider-ation of buoyancy provision among representativegenera of cyanobacteria and the variousmechanisms of its regulation, to an assessment oftheir functioning in natural environments and theirinfluence on observed distributions of cyanobac-teria, in time and space. These distributions arecorrelated with variations in the hydrodynamicstructure of the lakes in which the cyanobacteriagrow.

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380 New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21

COMPONENTS IN THE BUOYANTBEHAVIOUR OF CYANOBACTERIA

The primary requirement of photo-autotrophicmicro-organisms is to remain within or, periodic-ally, to gain access to, the insolated near-surfacelayers of lakes. To achieve this, they must eitherminimise the tendency, consequent upon the rela-tive density of their protoplasts (p' > 1000 kg m~3)to settle through the water; or, if the water circu-lation is vigorous and extends over a considerabledepth relative to the underwater penetration of lightenergy, to maximise the opportunities for entrain-ment within the upwelling currents and eddies.Given the extremes in the intensity of mixing andin underwater availability of photosyntheticallyactive radiation (PAR) among natural lakes (seeTable 1), as well as the temporal frequency of theirvariability (minutes to months), it becomes clearthat there is no universal attribute of phytoplank-ton cells that is ideal under all circumstances. Whilemotility can seem to cany obvious advantages inavoiding gravitational settlement, many non-motileplanktonic organisms nevertheless remain dis-persed through the vertical extent of the turbulent-mixed layer; so long as the velocities of the majorturbulent eddies (u) exceed, by one or more ordersof magnitude, the intrinsic settling velocities of theorganisms (ws), the cells are substantially trans-ported ("entrained"), both vertically and horizon-tally, within the flow (Reynolds 1984a).

The intrinsic settling velocity of an algal particleis generally assumed to conform to Stokes's law,such that:ws= 2 g r2 (P' — p)/(9 ij 0 (1)

where g is gravitational acceleration, p is the den-sity of the water and r\ its viscosity; p' is the den-sity of the organism and r is the radius of a sphereof identical volume; cf> is a shape factor, hithertoreferred to as "the coefficient of form resistance",which is evaluated only after all the other com-ponents have been determined, as the ratio betweenus, the calculated velocity of a sphere ($ = 1) of

the given volume and density, and the measuredvelocity, n-., (Oliver et al. 1981). Independent solu-tions for the form-resistance of such non-sphericalshapes as regular ellipsoids (McNown & Malaika1950), cylinders (Komar 1980), and chains ofspheres (Davey & Walsby 1985) are currentlyavailable. It should be noted that these formula-tions apply equally to buoyant particles: if p' < p,then w is negative; i.e., the particle floats upwards.

Size (r), shape (<t>) and density difference (p' — p)are, to differing extents, biological variables andsubject to adaptation in the cyanobacteria. Varia-tions in unit size and shape coincide with the typ-ical habits — which range through unicellularcoccoids (e.g., Synechococcus), mucilage-boundcolonial forms of varying complexity (e.g., Aphan-ocapsa, Gomphosphaeria, Microcystis), and fila-mentous structures that are either typically solitary(Oscillatoria, Spirulina) or aggregated into com-pound structures, such as bundles (Trichodes-mium), flakes (Aphanizomenori), or urchin-like balls{Gloeotrichia), held together in many instances bymucilaginous sheaths.

The contribution to excess cell density made byintracellular components such as proteins, con-densed carbohydrates, and polyphosphate bodiesmay be countered or overcome completely by thepossession of gas-vacuoles. There is now abundantevidence (Oliver & Walsby 1984; Thomas &Walsby 1985; Utkilen, Oliver & Walsby 1985) toshow that overall unit density is sufficiently sen-sitive to short-term fluctuation in the ballast con-tent and gas-filled space to bring about rapid (inthe order of 0.5-5 hours) reversals in density, fromp' > p to p' < p. The presence of a mucilaginoussheath damps the impact of changes in individualcell density but its volume contributes to anenhanced value of r (Walsby & Reynolds 1980). Inthis way, a small change in cell density may betranslated into a considerable change in buoyancy(positive or negative ws).

Algal entrainment in turbulent flow is facilitatedby the maintenance of a low value of ws relative to

Table 1 Ranges of variability in environmental factors influencing the suspension of phytoplanktonin lakes.

Variable Unit Range Reference

Current velocities («lDepth of mixing (zm)Mixing times (tm)

Surface PAR (/'<,)Daylength, 0-70° latitude (A)Coefficient of light attenuation (E)PAR availability of mixed layer (/*)

m s~ 'ms

umol m2 s~'s

m-i

mol d a y 1

0-0.30-2001O3-1O7

0-18000-86 4000 . 1 7 - > 8

0-60

Sutcliffe et al. (1963)Reynolds (1987a)Denman & Gargett (1983)Imberger (1985a)Harris (1978)List (1951)Reynolds (1987a)Reynolds (1987a)

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Reynolds et al.—Buoyancy regulation by cyanobacteria

need

the velocities of the major eddies (u).bulent transport is minimal u < ws), agments become dominated by the intrinsbehaviour. Maintenance within a favorange now depends upon almost neutral(p' < p). Owing to the relative infiexibitide size and shape, the inevitablerective adjustment is most readily mivariations in density. On the other handneed is for more frequent and morepensatory movements, such as in enwith a high frequency of alteration inadvantageous if density changes are oplarge particle size, where a small changibring about a significant alteration in w

We propose that these differing iiamong size, shape, and density in contrera are matched to the hydraulic condiiacterising the habitats in which each conoccurs (Table 2). Cyanobacteria with lo'velocities tend to occur principally inenvironments. A distinction may be drawnon one hand "picoplanktonic" forms,been most commonly encountered inlarge systems like the North American(Chang 1980; Sicko-Goad & Stoermer 8et al. 1985) and the open oceans (Johnburth 1979; Waterbury et al. 1979), andhand the solitary-filamentous formsOscillatoria) which dominate theexposed, optically-deep, shallow lake;1970; Gibson et al. 1971; Berger 1975)deeper lakes where seasonal mixingequivalent optical effects (Reynolds

Vhere tur-gal move-c buoyantred depthbuoyancyity of par-

for cor-t throughwhere the

lengthy com-ironments

m ixing, it isimised byin p' can

Great L

0 1

Table 2 Ranges of r, <p, p', and vv, (positivethe typical types of environments inhabited1, but departure from Stokes's law significan

381

teractionsasted gen-ions char-spicuouslyv intrinsicveil-mixedn betweenhich haverelatively

Lakes84; Caronon & Sie-the other

(especiallypi;inkton of

(Ahlgrenr occur ingenerates

1984a). Facul-

tatively rapid velocities distinguish the cyanobac-teria of more variable systems {Anabaena,Aphanizomenon, Microcystis) such as smaller,eutrophic lakes where the variations in mixing affectprincipally the euphotic layer (Reynolds & Walsby1975). Populations of large Microcystis colonies areespecially prevalent in warm lakes at lower lati-tudes and subject to diel cycles of mixing andstratification (Ganf 1974; Humphries & Imberger1982).

Other factors exert additional influences whichare not of principal concern here. It is importantto stress, however, that there is not only a trend inthe above series of decreasing susceptibility of dis-tribution to vertical mixing but there is also anincreasing requirement for self-regulation of buoy-ancy. In other words: the greater the capacity forthe expression of buoyant properties, so the greateris the need to be able to control buoyancy whenmixing intensity subsides. Frequent fluctuations inthe intensity and extent of vertical mixing demandrapid, short-term adjustments in the intrinsic sink-ing/flotation potential of suspended algae.

BUOYANCY REGULATION IN GAS-VACUOLATE CYANOBACTERIA

Short-term variations in cell density potentially offerthe most immediate responses to high-frequencyenvironmental fluctuations. There exist severalmechanisms for the regulation of density amongthe gas-vacuolate cyanobacteria; each is subject toclose physiological control.

linking rate or negative flotation rate) among various cyanobacteria andbased on literature values presented in Reynolds, 1987b). * nominally: at this size.

Species

Cyanodictyon

Synechococcus

Oscillatoria redekei

O. agardhii

Lyngbya limnetica

O. rubescens

Anabaena flos-aquaeAphanizomenon flos-aquae

Microcystis aeruginosa

r(um)

0.2-0.5

0.4-1.45

5.6-7.40

13.8-18.3

9.5-10.4

13.8-20.3

28-100up to 70

up to 120

up to 1000

up to 3200

4>

1

1.3

>5

10

10

6

1.71.5

1*

*

p' (kg m-3)

1040?

1040??

985-10857

990-1065920-1030920-1030

985-1005

_

( u r n s - ' )

< + 0.016

<+0.019

-0.8 to +5

? to +0.9

-0.7 to +7

- 6 0 to +10- 4 0 to +7

-360 to +120

+ 3000

+ 3300

Habitats

Open water picoplanktonof (generally) largeexposed lakes

Turbid, well-mixedshallow lakes

Deep lakes but stratifyingfor long periods

Epilimnia of temperatelakes in summer

Dielly stratifyingtropical lakes

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382 New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21

Kinetic regulation of gas-vacuole synthesisGas vacuoles comprise stacks of membranous cyl-inders called gas vesicles. The gas vesicles ofcyanobacteria vary in length from 200 nm to 2 urn,(with mean values of between 300 and 700 nm),and in diameter between 40 and 110 nm, but showlittle variation within any given species (Hayes &Walsby 1986). They are closed by conical endpieces. The particular protein making up the walls(gas-vesicle protein, or GVP: Walker et al. 1984) isassembled into ribs about 2 nm thick and spacedabout 4.5 nm apart.

Besides imparting rigidity, these proteinaceouswalls have an inner hydrophobic surface prevent-ing the ingress of liquid water but which is fullypermeable to gas. In life, the vesicles are filled withair, modified by intracellular metabolism, atapproximately atmospheric pressure; the compo-sition of the gas is less relevant to buoyancy thanis the maintenance of a gas-filled space per se. Nei-ther does the gas play any direct role in the infla-tion of the vesicle, which owes to the progressiveassembly of the double-coned structure and its sub-sequent enlargement to the diagnostic width andlength by the interpolation of GVP-ribs (Waaland& Branton 1969; Walsby 1975). This process isknown to take several hours, to complete; some 20-40 h may be required in which to erect, de now,sufficient gas vesicles to exceed neutral buoyancy(Reynolds 1987b).

As cells grow and divide, production of new gasvesicles must be maintained at equivalent rates ifthe buoyancy they impart is not to be progressively"diluted out". Growth and gas-vesicle synthesis arenot always closely coupled, it being possible for therelative gas-vesicle content of cells to increase ordecrease according to the rate of cell growth. How-ever, it is now apparent that gas-vesicle productionis independently regulated, especially in the popu-lations of cyanobacteria that commonly becomestratified in plate-like "depth-maxima" in stable,metalimnetic layers, some distance beneath thewater surface. Such stratification has been describedfor species of Oscillatoria of the O. prolifica-rubes-cens-agardhii complex (see Reynolds &, Walsby1975; Klemer 1976; Konopka 1984) in stratifying,temperate mesotrophic lakes but has been recog-nised in other solitary-habit genera {Dactylococ-copsis, Lyngbya) inhabiting stratified lakes at lowerlatitudes (Walsby et al. 1983; Reynolds et al 1983).In each case, stratification seems to provide a meansof conserving biomass with minimum energyexpenditure through a period in which growth inthe epilimnion is severely limited by nutrient defi-ciencies. Stratification deep in the light-gradientensures that photosynthetic carbon fixation is bet-ter matched to the supply of other nutrients (espe-

cially phosphorus, nitrogen) available to supportgrowth.

The maintenance of stratified layers dependsupon the organisms' ability to remain neutrallybuoyant, while morphological constraints (r small,<p large) determine that any vertical movements arealways slow (see Table 2). Because the rates ofgrowth of deeply stratified populations are often low(Walsby & Klemer 1974; Lund & Reynolds 1982),gas-vesicle production is likely also to be corre-spondingly restricted (Utkilen, Oliver & Walsby1985). Moreover, if additional supplies of limitingnutrients are made available to stratified popula-tions, Oscillatoria spp. will move up to a new posi-tion in the light gradient where a new balancebetween carbon fixation rates and nutrient avail-ability may be struck (Klemer 1976, 1978; Klemeret al. 1982). Presumably, this upward migrationcould depend, in part, upon renewed gas-vesiclesynthesis.

The turgor-collapse mechanism

Although the structure of their walls imparts rig-idity to the intact vesicles, the volume of which isrelatively unaffected by hydrostatic pressures ofseveral bars (Walsby 1982), vesicles will neverthe-less collapse irreversibly once a certain criticalpressure is exceeded. External pressures sufficientto collapse intact vesicles isolated from cyanobac-terial cells vary interspecifically and over widerranges: 0.4-0.8 MPa in Anabaena flos-aquae ; 0.6-1.1 MPa in Microcystis aeruginosa; 0.7-1.2MPain Oscillatoria spp.; and up to 3.7 MPa in themarine Trichodesmium thiebautii (references citedin Hayes & Walsby 1986). Moreover, the meancritical pressures of vesicles from different speciesare inversely correlated with their characteristicdiameters (Hayes & Walsby 1986), each speciesproducing gas vesicles of the maximum widthcompatible with the strength required to collapseby the pressures typically encountered in theirnatural environments (Walsby 1975). These struc-tural differences may be prescribed by minor differ-ences in the amino acid sequences of the particularGVP from which they are assembled (Walker et al.1984). Because the gas vesicles within living cellsare already subject to internal osmotic pressures(or cell turgor) of 0.3-0.4 MPa, augmented byincreasing hydrostatic pressure with increasingdepth beneath the water surface (0.011 MPa m"1),their collapse is effected by the application of cor-respondingly lower external pressures. Walsby's(1969) original observation that a laboratory strainof Anabaena flos-aquae became buoyant whenmaintained at low light intensity but lost buoyancywithin an hour of transfer to high-light was shownsubsequently to be due to the collapse of a pro-

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Reynolds et al.—Buoyancy regulation b

portion of the gas-vesicles in responsecell turgor of 0.1 MPa (Dinsdale & WiOliver & Walsby 1984). The increased tisure is generated partly by the photosynduction of low molecular weight carl(Grant & Walsby 1977) and partly bdependent uptake of potassium ionsWalsby 1981). Photosyntheticallyreversals in the buoyancy of naturallyAnabaena circinalis have been shownwithin 2-4 h when held in bottles suspethe lake surface (Reynolds 1975). Suchmay be invoked to account for dielmovements observed in a number of infield observations on populations of An,Aphanizomenon (reviewed by ReynolEven where turbulent mixing velociexceeds the migratory velocity, recoveritical series of upward- and downwid-openisediment traps attest to the continued re:buoyancy (Reynolds 1975, 1976).

Accumulation of condensed carbohydra

Photosynthetically fixed carbon is accuicyanobacterial cells in the form of glycsity 1500 kg m 3) which adds to the exoof the cells (Utkilen, Oliver & Walsby 19contributing to buoyancy loss in actisynthesising cells of Anabaena, it has 1recently that the accumulation of cai"ballast" provides the main mechanismregulation in Microcystis (Kromkamp &Thomas & Walsby 1985): the turgor riseto 0.35 MPa) observed by Thomas & W<suspensions were transferred(<1 nmol m-2 s"') to high (>60um(irradiances was insufficient to collapsecant proportion of the gas vesicles preseother hand, the observation that glycogof cells is varied considerably in the(Cmiech 1981; Reynolds et al. 1981shown to be quantitatively significant ibalancithe buoyancy contributed by the existircles. The gas vesicle content of Microalters over longer periods (days to weeksto ambient environmental conditions, si:potential for short-term density contnspondingly altered (Reynolds et al. 198al. 1985).

Interactions of buoyancy regulation witlimitation

While the rate of photosynthetic carboiessentially governed by the light intensithe cell is exposed, accumulation of phiis also subject to light-independent assiir

cyanobacteria 383

a rise insby 1972;rgor pres-hetic pro-ohydratesthe light-Mlison &mediatedoccurringto occur

ided nearbehaviourmigratoryiependent>aena ands 1987b).y greatlys in a ver-d-opening[ulation of

ulated in>gen (den-ss density5). Beside:ly photo-:n shownbohydrateof densityVlur 1984;from 0.27sby whenm low

iny signifi-nt. On thegn contenthort termhas beenbalancing

g gas vesi-oystis cellsaccording:h that the

is corre-Oliver et

nutrient

ixation isto which

;osynthatelation into

proteins and other biopolymers, assuming that otherinorganic components are available. Thus, thecapacity to accumulate soluble, low molecularweight sugars and polysaccharide interacts withnutrient availability, the key control being the rela-tionship between carbon fixation and utilisation(Konopka 1984). Evidence for this interaction hasbeen obtained from field and laboratory studies.The addition of NH4NO3 to populations of Oscil-latoria agardhii var. isothrix enclosed in in situ col-umns (Klemer 1973) or bottles (Walsby & Klemer1974) resulted in increased buoyancy. Booker &Walsby (1981) used an experimental laboratorywater column to demonstrate that when grown in"complete" medium, Anabaena flos-aquae becameextremely buoyant and aggregated at the surface,whereas under either phosphate or sulphate limi-tation the organisms stratified at a depth of c. 1 m.Klemer et al. (1982) used cyclostats to demonstratethat carbon and nitrogen limitation have oppositeeffects on the buoyancy of Oscillatoria rubescens,nitrogen limitation resulting in a decreased gas vac-uolation while transition to carbon limitationbrought about increased vacuolation. These changesin gas vacuolation resulted in the loss or gain ofbuoyancy.

Both the turgor rise mechanism and the accu-mulation of carbohydrate are dependent on theavailability of CO2 for photosynthesis and it hasbeen demonstrated that limitation of CO2 preventscells from losing buoyancy and promotes bloomformation (Dinsdale & Walsby 1972, Reynolds &Walsby 1975; Walsby & Booker 1980). Direct evi-dence has come from the cyclostat experiments ofKlemer et al. (1982) who found increased gas vac-uolation in Oscillatoria under C limitation. Walsby& Booker (1976) found less surface accumulationof A. flos-aquae in the half of a partitioned labora-tory-column treated with carbonate while Paerl &Ustach (1982) found that the buoyancy of Aphan-izomenon flos-aquae was highest under CO2-lim-iting conditions. Other conditions which reduce thecarbon fixation rate are also likely to result in sur-face blooms, possibilities include cell senescenceand photo-oxidation of pigments (Reynolds &Walsby 1975).

Comparison of buoyancy-regulating mechanismsThe relative importance of the three mechanismsof density regulation — gas vesicle production andgrowth dilution, collapse by turgor pressure, andcarbohydrate accumulation — varies in differentgenera and species of cyanobacteria. These differ-ences in buoyancy control and the differences inthe potential travel distances that a given adjust-ment in buoyancy may effect are summarised inFig. 1.

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384 New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21

Synecho-coccus

Oscillatoria Anabaena Microcystis

High

i

Low

B

o>

O

/o

160-

°-120m§ en

Anabaena Oscillatoria Microcystis

Low High Low High Low High

80-

ça bS = 40-n o00 >

0J

Fig. 1 A, Diagrammatic summary of the means andeffects of buoyancy regulation in a selection of cyano-bacteria of different sizes: open rhombi denote gas vacu-oles; solid circles, glycogen; arrows represent direction ofmovement in water and relative distances travelled perunit time. B, Quantitative values of cellular ballast, cal-culated as the weight of constituent minus the weight ofwater displaced, attributable to carbohydrate (solid), pro-tein (cross hatching) polyphosphate bodies (vertical hatch)and, in Microcystis, to extracellular mucilage (stipple), andof the "negative ballast" contributed by gas vesicle space(open figures) in selected cyanobacteria, as grown under"low" light (15 umol m"2s"1) intensity and 7-24 hoursafter transfer to "high" light (>50 umol m~2 s~')- Origi-nal data from Oliver & Walsby (1984), Utkilen et al.(1985a), and Thomas & Walsby (1985); redrawn fromReynolds (1987b: fig. 3 and 6).

Table 3 Typical buoyancy-adjustment times (^ in s)achieved through the different regulation mechanisms.

MechanismTime to lose

buoyancyTime to recover

buoyancy

Vesicle production 10s-106 105

and growth dilutionTurgor collapse 103-104 105

Ballast control > 104 > 104

These buoyancy-regulating mechanisms also dif-fer in the time scales of their responses. Kineticregulation of gas vesicle synthesis may permit non-growing cells to develop buoyancy within a day orso (~105 s), probably longer if the cells are alsogrowing rapidly. Conversely, the rates of "dilu-tion" of non-replicating gas vesicles among daugh-ter cells will be scaled to the cell generation time,in the order of 1 to 10 days (105-106 s). In contrast,the turgor-collapse mechanism permits activelyphotosynthesising cells to begin reducing buoyancyas soon as internal turgor exceeds the critical pres-sures of the weakest vesicles present; in practice,healthy cells of Anabaena, already close to neutralbuoyancy, may start sinking within 20 min to 3 h(10M0 4 s); however, recovery of buoyancy dependsupon the production of new vesicles (~105 s, above).Adjustment of carbohydrate ballast alone offersequivalent rates of rapid buoyancy loss and recov-ery, which are primarily dependent upon the con-temporaneous cell-specific rates of photosyntheticproduction and respiration. Again, in healthypopulations of Microcystis, maintained at temper-atures of 20°C, reversals in buoyancy can be broughtabout within 4-12 h, or 1-4 X 104 s (Reynolds etal. 1981).

These time scales, summarised in Table 3, areliable to extension in nutrient-limited populations.Their significance must be viewed in relation to thefrequencies of variability in the underwater light-environment.

BUOYANCY REGULATION IN NATURALENVIRONMENTS

Distribution in relation to physical variabilitySince Reynolds & Walsby (1975) attempted to relatethe occurrence of different cyanobacterial popula-tions to within- and between-lake differences inphysical structure and variability, considerableprogress has been made in the empirical descrip-tion of limnetic water movements at the scalesexperienced by individual planktonic organisms.Recent accounts of the time and space scales ofdiffusive displacement in turbulent flow includethose of Abbott et al. (1982); Humphries & Imber-ger (1982); Denman & Gargett (1983); Powell et al.(1984); Imberger (1985b). The limnetic motionsgenerated by the Earth's rotation (Coriolis force),gravitational throughflow, and convection (causedby alternative heating and cooling at the water sur-face) are variably augmented by kinetic energyintroduced by wind stress at the surface, inducingwaves, Langmuir circulations, deeper return flowsand a "spectrum" of intermediate eddies. Theproperties of the wind-mixed layer are related tothe rate of gain of mechanical energy at the surface

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Reynolds et al.—Buoyancy regulation

and to the stability gained by the net aisorption ofsolar radiation. Absorption of heat by sirface waterscauses expansion and, hence, a reductin in densityp. The tendency of this warmer water ) float uponthe colder, denser water below brings bout a den-sity stratification, the stability of which : s expressedby the Brunt-Vaisala or buoyancy ;quency, N(units: radians s~')> and calculated direitly from thegradient of density with depth:N2 = (g/p)(dp/dz)

The effect of vertical mixing is to sdevelopment of the density gradient,moderate winds on the water surface ge:stress, expressed as the correlationhorizontal (w') and vertical (Wcomponents:

Tie

p u w = pu^where p uj (units: N m~2) is the(equivalent to T in Spigel & Imberge1

represents the shear or friction veacisurface waters. The interaction of thewith the vertical gradient of horizon{du/dz) is the primary source of mixcd-lbulence. The force available to carrymixing is equivalent to p u,2L (unitswhere L is the length of the basin in t e directionof the wind. Except at low wind speeis, the hori-zontal shear velocity u^ is a direct cornl ate of windspeed (Sutclifte et al. 1963).

In the absence of buoyancy effects l e extent ofmixing is determined only by the velocity scale, u#,and the velocity gradient (du/dz):h = uj(du/dz) (4)

where h is the mixed-layer depth. Whe•e buoyancyforces inhibit full mixing, however, turbulent eddiesare confined to a near-surface layer, This upper,mixed layer is relatively uniform in dnsity but itslower boundary is a more or less ab"upt densitygradient. The buoyancy force maintainng the iden-tity of mixed layer is more appropriatly expressedby the difference between its density and that ofthe water immediately beneath it, or , p . Its thick-ness depends upon the ratio of the toloyant forceto the mechanical energy available, his ratio isgiven by the (dimensionless) Wedderbirn number,W, (Imberger & Hamblin 1982), the v, ue of whichusefully summarises the general behadour of themixed layer.

(5).

For values of W > 1, little deepening af the mixedlayer will occur when subjected to increased wind-stress; where W < 1, the stratification is sensitiveto mixing episodes and liable to rapd deepening(see Spigel & Imberger 1987).

cyanobacteria 385

(2).

ppress theaction of

erates shearetween the

velocity

(3),

hear stress1987), andacity in the

shear stressl velocitiesd-layer tur-out vertical

This consideration introduces three quantities ofrelevance to the distribution of planktonic cyano-bacteria within lakes: uv h, and W.

um (m s"1), the average turbulent velocity, is directlyrelated to windspeed U through the relation:

P i c U 2 = p u S (6)

where p and paare the densities of the water andair (respectively, 1000 and 1.2 kg m"3) and c isa coefficient of drag, 1.3 X 10~3 (Denman &Gargett 1983). Thus, windspeeds of >4 m s~'are sufficient to generate values of u^(>0.005ms-') which exceed the maximumsinking and floating velocities of any cyanobac-terium listed in Table 2. Planktonic populationsare generally liable to full dispersion throughwind-mixed layers (see also George & Edwards1976).

h (m) is the vertical extent of the mixed layer. Inthe absence of density stratification, turbulentmixing may extend 100-200 m beneath the sur-face. This is an extreme value, and in manylakes, the maximum mixed depth (h) is con-strained by the size and depth of the basin. Atthe other extreme, h may shrink to a few mil-limetres. At intermediate values of h, deter-mined by the density stratification, it isimportant to recognise that while cyanobacteriaremain generally dispersed through the mixedlayer, they may progressively sink or floatthrough, or maintain station within, the ther-mally stratified water column below.

W, the Wedderburn number itself, describes thestability of a given structure.

Equation (5) can be solved to predict the maxi-mum depth of the mixed layer of a stratified sys-tem that will satisfy the stability condition W > 1.Giving appropriate values to g (9.81 m s 2), Ap(0.5 kg m 3, equivalent to the density differencebetween water masses at 10 and 20 °C), p(1000 kg m 3 ) and u^ (0 .01ms 1 , the turbulentvelocity generated by a windspeed of 8ms~>),g&pKpu^2 may be solved at c. 50 m~ ' . Thus,h2/L > 0.02 m for the condition to be satisfied. Fora small lake (L =) 1 km across, the mixed depth(h) may be up to 4.5 m. For a larger lake, 100 kmacross, it is closer to 45 m. In either case, the mix-ing depth is significantly reduced during warm, calmweather but, while all other factors remain con-stant, the value of W is substantially reduced. Theimplication is that large lakes are subject to largefluctuations in the intensity and absolute depth ofturbulent mixing. Persistent periods of near-surfacestability are generally a feature of smaller or warmerlakes in which populations of bloom-formingcyanobacteria are often observed to flourish.

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386 New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21

Mixing timesDenman & Gargett (1983) give examples of the timetaken for wind-driven fronts to traverse the mixed-layer depth h under differing shear velocities at thewater surface. This "mixing time" ?m, is given bythe quotient h/u^, since both the mixed depth andshear velocity are correlates of wind speed (U), tmvaries less than the variation in U, falling withinthe range 4-50 minutes (2 X 102 to 3 X 103 s). Inthe absence of vertical density gradients, or in shal-low lakes where the depth of wind mixing is limi-ted by the absolute depth, different solutions of tmwill apply (Denman & Gargett 1983). Nevertheless,it is the order of magnitude of the estimate whichis relevant: at low wind speeds, where penetrativeconvection, Coriolis forces, and residual wavemotion dominate water movement in the verticalplane, or below the base of the mixed layer (thethermocline), mixing times substantially increaseto the order of days to months (105-107s; seeImberger 1985a).

The intrinsic movements of planktonic organ-isms can be expressed in corresponding dimen-sions. Whereas an Oscillatoria filament, sinking orfloating at a constant vertical velocity of3 X 10~6 m s" < would require 5 X 106 s (or 58 days)to clear a static column of 15 m, a large Microcystiscolony (ws = 3 X 10~3 m s~">) in the same columnwould have a clearance time (tc) of 5 X 103 s, orabout 1.5 hours.

Besides expressing the interaction of intrinsicbuoyant properties and turbulent mixing, the ratiotm/tc indicates the immediate; repercussions so faras vertical distribution is concerned. In the case ofthe well-mixed 15m column above, the verticaldistribution of buoyant trichomes of Oscillatoria(We = 2X103/ 5X106 = 4X10-") is unlikely tobecome differentiated but the intensity of mixingwould barely exceed the tendency of buoyantMicrocystis colonies to accumulate towards the topof the layer (tm/tc = 0.4). Colonies transported tothe base of the mixed layer would rapidly recoverposition (106 s/5X103 s = 200) but Oscillatoria tri-chomes regulating buoyancy to one part in 20(Walsby & Klemer 1974: ws~0.3X l O ^ m s • ;tm/tc ~ 0.3) would be capable of maintaining stationthere and a net accumulation, as in a depth-maxi-mum, would become manifest.

The relative advantages to growth and survivaloffered by these strikingly different buoyant behav-iours depend very much upon the limnologicalconditions obtaining in given lakes, which includethe manner in which other potential growth-regu-lating factors and resources are distributed withdepth.

Photoperiods in mixed layers

One of the major consequences for organismsentrained in vertical mixing is the variation in thephoton flux density perceived.

If Ik is the intensity required to saturate the pho-tosynthetic capacity of an autotrophic organism,then the proportion of time in which an activelymixed population will experience saturation is indirect proportion to the fraction of the mixed layerdepth, h, that lies above the depth at which 7kobtains. Beneath the depth of 7k, photosyntheticpotential is directly limited by the gradient ofdeclining irradiance, until ultimately the availablelight fails to support net photosynthetic gain at all.This depth, the compensation point, may be refer-red to as zcand the vertical height from the surfaceto zc will be called hc. Clearly, if h < hc, and 7k islower than the intensity obtaining at the base of h,much of the exploitable light field also lies belowthe mixed depth. In these lower euphotic depths,gas vacuolate cyanobacteria are potentially able tocontrol their vertical position. If h ~ hc, the popu-lation now receives a lower overall light dose, butthere is no point where net photosynthesis is pre-vented by the mixing. In other words, the lightperiod experienced by the mixed-layer populationremains identical to the day length. However, ifhc< h part of the mixed population is, at any time,in effective darkness, although the vertical mixingshould continue to carry cells into and out of thelight.

For the organisms there are two important con-sequences of this effect. One is that the total day-light period is shortened. The other is that the light-dark alternations increase in frequency. The pho-toperiod (tp) is given by hju^ or tm (hc/h). For mix-ing times of 30 min through a turbid layer, in which(say) hjh = 0.33, tp is only 10 min (0.6 X 103 s).Unlike cases in which hc> h and ^ corresponds tothe length of the solar day (say, up to 15 h or5 X 104 s), mixing through turbid layers restrictsthe opportunity for cyanobacteria to reverse theirbuoyancy (tp < tb). However, they may wellrespond to the lowered total daily light dose (thesum duration of photoperiods X the mean irra-diance level) through adjustment between thekinetics of growth and gas vesicle production.

Interactions between response times and mixingtimes

Several contingencies relating to physical environ-ments may now be proposed which might discrim-inate between the buoyancy adaptations of thecyanobacteria. The principal interactions concernthe extent of turbulent entrainment and the oppor-tunities for buoyancy-regulated movements to

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by cyanobacteriaReynolds et al.—Buoyancy regulation

occur. These possibilities are usefully <Misidered interms of comparative time scales, wlich may bearranged in various hierarchies.

Let us first consider well-mixed envronments inwhich h > 10 m or so. With a concimitant highclarity {hc > h), we may assert that:

tm<th< tp (7).

Here, buoyancy regulation can have little effect,save to prolong the residence, tc, withii the motionso that tc > tp. This may also be achiived by hav-ing a small unit size. Indeed, the maj jrity of uni-cellular species of algae, non-motik as well asmotile, should be expected to thrive i clear, well-mixed lakes and epilimnia: chroooiccoid pico-plankton are found particularly nder theseconditions.

In productive waters, potentially upporting ahigh phytoplankton biomass, light nergy maybecome the limiting factor. As argued ibove, muchof the mixed layer may be in effective darkness, sothat:

(8).

In this instance, buoyancy regulation h s little effect,although maintenance of a positive bubyancy, pro-vided by gas vesicles of relatively high strength,serve to prolong tc Such adaptations characteriseOscillatoria sp.

Waters with high physical stability and shallowmixed layers (h < 2 m) may nevertheless supportsufficient concentration of biomass far hierarchy(8) to apply. In many instances, however, h < hcthis means that a considerable depth of non-tur-bulent water exists beneath a superficial layer ofconstrained turbulence. So long as tiis structurepersists, the effective mixing time of the non-tur-bulent layer extends to days or weeks. Thus:

andFrequent adjustments of buoyancyregulated movements are possible. Idcome of these movements would beindefinitely. These habitats areexploited by large aggregating or colo(e.g., Anabaena and Microcystis).

Mention may also be made of cyilakes which regularly stratify by daymixed by afternoon winds or penetr;tivecontion overnight (e.g., Ganf 1974; PoweImberger 1985b). During part of the

tb < 'm <tp

and, during mixing,

(tp or tm)

387

(9).

buoyancy-ally, the out-to extend tcparticularlyial forms of

les in warmand becometive convec-

et al. 1984;ay,

(10)

(11).

Again, the effect of buoyancy adjustments duringthe diurnal stratification will be to restore thepopulation to the insolated portion of the column,thus prolonging tc. Here, close control of density ofthe organisms, coupled with rapid, buoyancy-con-trolled movements favours algae with large unit sizeand light-sensitive regulation especially associatedwith Microcystis colonies.

In addition, it might be added that continuedgrowth in turbid, mixed columns also depends uponenhanced light harvesting mechanisms (morphol-ogical attenuation, increase in cell-specific chloro-phyll content and increase in accessory pigments),so that the limited opportunities to support netphotosynthetic production are exploited accord-ingly. It is interesting to speculate that, among thecyanobacteria, these properties of "low-light adap-tation" reach their highest development amongsome of the Oscillatoria spp. (Utkilen, Skulberg &Walsby 1985); in contrast, the light-limited pho-tosynthetic efficiencies of some bloom-forminggenera (e.g., Microcystis) are much lower (see Rey-nolds 1987b). These seem more suited to longerphotoperiods (several hours). It may be that theseforms are also able to tolerate the higher lightintensities during the day, hc > h, possibly abettedby buoyancy-regulated migrations. However, low-light adapted Oscillatoria trichomes, placed insaturating light intensities for periods of over onehour or so, seem certain to become photo-inhibitedand to suffer severe physiological stress (Harris1978). It seems likely that there is a further timescale (for convenience, Q which would describe thefrequency of irradiance fluctuations to which theorganism had adapted; it would be expected that4 would have a periodicity similar to tp. In the con-text of the distributions of various cyanobacteria,this is a topic deserving further consideration.

INTERACTIONS OF BUOYANCY WITHGROWTH-REGULATING FACTORS INNATURAL ENVIRONMENTS

Buoyancy regulation, including its impact uponvertical and horizontal distribution with respect towater movements in natural environments, is onlyone of a large number of ecological factors influ-encing the occurrence and frequent dominance ofcyanobacteria in the plankton. Effects of tempera-ture, light, and availability and uptake of majornutrients and various micronutrients, together withbiotic interactions with other micro-organisms,grazers, parasites, and pathogens, are consideredelsewhere in this issue. To varying extents, therespective influences of these factors on the popu-lation dynamics of cyanobacteria nevertheless

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388 New Zealand Journal of Marine and Freshwater Research, 1987, Vol. 21

interact with, or are modified by, the nature andextent of mixing processes within natural waters.In a recent review, Reynolds (1987b) surveyed theavailable literature on the growth of several keygenera of planktonic cyanobacteria in relation totemperature, light, and nutrient availability, in aseries of hypothetical environments. The optimalenvironmental conditions that were contrived pro-vided a surface layer, gently mixed to a depth thatremained within the range of light saturation ofphotosynthesis and which was charged with allmajor and trace nutrients (including carbon diox-ide) at concentrations saturating the knownrequirements of phytoplankton. The temperatureof this layer was arbitrarily set at 20 ( + 2) °C anda daylight period of 16 h was adopted as a realisticrepresentation of the daylength experienced bytemperate lakes at the time of the summer solstice.The series of idealised environments was developedby selectively lowering each of the resource com-ponents in turn to subsaturating levels, distinguish-ing between those effects which were attributableto the (autogenic, density-dependent) impact ofphytoplankton growth, e.g., reduced light penetra-tion through the mixed layer and the depletion ofdissolved nutrients, and those (allogenic, density-independent) consequences of (for example)increased depth of mixing or the resticted supplyof one or more essential nutrients.

Whereas the maximal growth rates (^max = 0.6-0.8 day 1 ) of most colonial and filamentous cyano-bacteria are inferior to those of small, non-motileunicellular members of the Chlorophyta (e.g.,Ankyra, Chlorella: 1.4day"1) under the optimalfield conditions proposed, the superior light-har-vesting properties of filamentous cyanobacteria(notably of Oscillatoria) become advantageous whenmixing consistently extended beyond the depth ofpenetration of saturating irradiamce, while thesuperior affinities and storage capacities of colonialforms (e.g., of Microcystis) render them lessimmediately dependent upon external nutrientsupplies than the majority of potentially faster-growing small algae. Moreover, the resistance ofthe larger, gas-vacuolate colony-forming cyanobac-teria to sinking loss or consumption by grazers canprovide a significant advantage when these factorsoperate against small, non-motile unicellular andcoenobial phytoplankton. Such reasoning isdeveloped more fully in Reynolds' (1987b) review,which concludes that if suboptimal environmentalconditions persist and the structure of the phyto-plankton population evolves along an ecologicalsuccession, there is a high probability that thesequence will approach a climactic equilibriumdominated by a cyanobacterial species (Reynolds1980; 1984b). Examples include enriched shallow

lakes of well-mixed temperate (assemblages dom-inated by O. agardhii - O. redekei) and tropicallakes (Spirulina, Lyngbya spp.), and in deeper tem-perate {Oscillatoria rubescens) and subtropical sys-tems {Microcystis). Among tropical lakes,commonly observed diel alterations of thermalstratification and mixing represent a level of envi-ronmental constancy which may select in favour ofMicrocystis dominance. Waters which are chroni-cally deficient in sources of combined inorganicnitrogen tend to select in favour of nitrogen-fixinggenera (e.g., Anabaena, Aphanizomenon, Cylin-drospermopsis spp.) while among brackish waters,the advantage may fall to species of Nodularia(Ostrom 1976; Huber 1984).

CONCLUSION

Perhaps the most remarkable feature of the plank-tonic cyanobacteria is the diversity of their mor-phological, physiological, and behaviouraladaptations. Whilst sharing the same basic pro-karyotic structural organisation, cells vary inter-specifically in size and shape and, especially, in theways in which they comprise secondary structures,ranging from straight filaments to mucilaginouscolonies. We have shown how these characters maybe combined in ways which are each suited to par-ticular environmental conditions, arising fromdifferences in hydrodynamic structure and theavailability of resources in lakes.

Dominance by cyanobacteria can result from avariety of interactions among constraining envi-ronmental factors. The differing adaptations ofcyanobacteria collectively contribute to the abilityof the group to exploit a very wide spectrum ofenvironmental variability, in the broadest sense; itis perhaps this range of evolutionary strategies,variously adopted by individual species of cyano-bacteria, that earns their reputation as a prominentand successful group of organisms.

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1982: The elastic compressibility of gas vesi-cles. Proceedings of the Royal Society of London B216: 355-368.

Walsby, A. E.; Booker, M. J. 1976: Stratification andbloom formation by planktonic blue-green algae.In: Codd, G. A.; Stewart, W. D. P. ed., Proceedingsof the second international Symposium on Pho-tosynthetic Prokaryotes. Dundee, FEMS, pp. 11-12.

1980: Changes in buoyancy of a planktonicblue-green alga in response to light intensity. Brit-ish phycological journal 15: 311-319.

Walsby, A. E.; Klemer, A. R. 1974: The role of gas vacu-oles in the microstratification of a population ofOscillatoria agardhii var. isothrix in Deming Lake,Minnesota. Archiv far Hydrobiologie 74: 375-392.

Walsby, A. E.; Reynolds, C. S. 1980: Sinking and floating.In: Morris, I. ed., The physiological ecology ofphytoplankton, pp. 317-412. Oxford, BlackwellScientific Publications.

Walsby, A. E.; van Rijn, J.; Cohen, Y. 1983: The biologyof a new gas-vacuolate cyanobacterium, Dactylo-coccopsis salina spec. nov. in Solar Lake. Proceed-ings of the Royal Society of London B 217: 417-447.

Waterbury, J. B.; Watson, W. S.; Guillard, R. R. L.; Brand,L. E. 1979: Widespread occurrence of a unicellular,marine, planktonic cyanobacterium. Nature 277 :293-294.

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