HOLARCTIC ECOLOGY 3: 141-159. Copenhagen 1980

Phytoplankton assemblages and their periodicity in stratifyinglake systems

Colin S. Reynolds

Reynolds, C. S. 1980. Phytoplankton assemblages and their periodicity in stratifyinglake systems. - Holarct. Ecol. 3: 141-159.

A subjective analysis of the seasonal periodicity of phytoplankion populations inseveral natural lakes and experimental lake systems (Lund Tubes) has shown that thedirection and patterns of change are both general and predictable. The paper distin-guishes between autogenic successional changes, consistent with increasing com-munity complexity and segregation, and allcgenic changes resulting from turbulentdisruption of the stratified system. The periodicity of the assemblages recognized isresolved through the interaction of two major variables - nutrient availability andcolumn stability. A simple possibility matrix is proposed which can account for theobserved changes in community structure. The principal paihways in eulrophic lakes(diatoms -^ Volcocales —* Nostocalcs -+ dinoflagellates or Microcystis. with rever-sions through 'summer diatom' assemblages) and in mesotrophic lakes (diatoms —*Chrysophyte/Sphaerocysiis -+ dinoflagellates. with reversions through 'summerdiatom-desmid' assemblages) are generally consistent with the growth and survivalstrategies of the principal algal species concerned.

C. S. Reynolds, Freshwater Biological Association, Windermere Laboratory,Ambleside, Cumbria LA22 OLP. U.K.

1. Introduction

In many of those lakes whose phytoplankton has beenmonitored intetisively over several consecutive seasotis,distinctive seasonal fluctuations in aigal biotnass havebeen demonstrated. The individual species which be-come dominant in a given lake are relatively few itinumber, and these same species are often themselvesnumerous in an annually recurring sequence. This pat-tern is usually termed "the seasonal succession" of thephytoplankton. Moreover, the sequence of dominantforms, at least in terms of the taxonomic classes of algaethey represent, is often similar in different lakes sharitigsimilar morphometric and chemical properties (cf.Reynolds 1973a, Stoermer 1978). These similaritiessuggest that seasonal succession may be generally sub-ject to overriding interactions of a relatively smallnumber of environmental variables. Factors which havebeen shown to influence the specific composition ofphytoplankton include day length and average light in-tensity (Foy et al. 1976, Wall and Briand 1979), temp-erature (Hammer 1964, Patrick 1969), nutrient uptake

kinetics (Tilman and Kilham 1976, Tilman 1977),grazing by zooplankton (Nauwerck 1963, Haney 1973,Porter 1977), sinking (Lund et al. 1963, Lund 1966.Reynolds 1973b, 1976a, Knoechel and Kalff 1975).pathogenic infections by protozoa, fungi and viruses(Canter 1972, Safferman and Morris 1967) and al-lelopathy (Keating 1977).

Despite the existence of a large and expanding lit-erature describing seasonal succession, including anumber of valuable review papers (e.g. Lund 1965,Round 1971, Fogg 1975, Porter 1977), progress to-wards producing either a generalized hypothesis to ac-count for seasonal succession or a basis for the predic-tion of successional events has been slow. Importantconceptual advances have recently been made by Mar-galef (1978) whose work is largely directed towards themarine phytoplankton, and by Lewis (e.g. 1978a, b), inhis exhaustive analysis of data from the tropical LakeLanao (Mindanao, Philippines). Both authors have de-monstrated the response of phytoplankton communities

Accepted 15 February 1980© HOLARCTIC ECOLOGY OI05-9327/80/030t4t-19 S O2.5O('O

HOLARCTIC ECOLOGY y.i (1980) 141

to stable thermal stratification and nutrient depletionwithin the trophogenic zone, and to the effects of tur-bulent breakdown of stratification (see also Reynolds1976b, c). The precise nature of the response is influ-enced by the physiological characteristics and ecologicaladaptability of the individual species concerned (see, forinstance, Harris 1978, Kalff and Knoechel 1978).

These concepts form the basis of the present paper,the aim of which is to establish that the responses ofcommunities in five contrasted lake systems are bothgeneral and predictable. The approach I have adopted issummarized. Initially, the nature and terminology of thechanges are discussed (Sect. 2), and the methodsemployed in their investigation are outlined (Sect. 3). Aphytosociological analysis identifies fourteen groups ofcommonly-associated species (assemblages), which areused to rationalize the description of compositionalchanges (Sect. 4). The temporal sequences of the as-semblages are then related to the occurrence of majorvariations in the ambient environmental conditions(Sect. 5, 6). Finally, the periodicity of the phyto-plankton is briefly reviewed in terms of specificstrategies for growth and survival (Sect. 7).

My remarks are confined to the stratifying systems onwhich the qualitative analysis is founded, and in whichfluctuations in physical structure are relatively well de-fined. Doubtless, many of the conclusions may apply toplankton periodicity in shallow, mixed systems, includ-ing rivers (which often shows certain similarities withthe cycles in deeper lakes), but I consider that detailedcomparison is beyond the scope of the current work.

2. Theoretical considerations of succession

Some initial clarification of the use of the term "succes-sion" is desirable. The classical concepts of successionhave been evolved mainly in terrestrial plant ecology;an area of the earth's surface is successively invaded andmodified by recognizable communities, tending througha series of predictable, distinctive stages from 'pioneer'to 'climax' associations (e.g. Odum 1971). The annualcyclical progression of phytoplankton species in a fluidenvironment does not coincide exactly with this tradi-tional view. Yet there are sufficient identifiablesimilarities (e.g. increasing complexity, diversity andcrop, and declining productivity) in both progressions(Margalef 1968) to validate the comparison. The classi-cal view of succession also implies (and, indeed, de-pends upon) a strongly directional component, but thisis still not well-defined for the observable changes inphytoplankton composition occurring In lakes (cf. Lewis1978a). Margalef (1978) has argued that the "mainsequence' of phytoplankton succession is governed bythe interactions between (a) developing organizationwithin the ecosystem, arising as a consequence of ther-mal stability and the downward depletion of nutrients.

and (b) the morphological and physiological adapta-tions of the planktonic algae (In combining mechanismsfor remaining in suspension and for maximising nutrientuptake) to exploit it. Margalef hypothesised that the"main sequence" would be from small to larger species,and from nonmotile to motile ones. Seasonal variationsin the composition of the freshwater phytoplankton donot always conform to this pattern, however. In lakes,the relative fluctuations in thermal stability and nutrientavailability occur on a fmer scale and are invariablymore frequent and more rapid than is typical for the sea.Lewis (1978a) has argued that the rates of change in thephytoplankton community may be equally rapid inlakes, but often lack the directionality described byMargalef.

Classical serai successions (such as that from bareground to a forest ecosystem) are nevertheless liable toreversion to earlier successional stages as a direct resultof an environmental perturbation (in this example, say,clear-felling) or to maintenance in a state of plagio-climax (say, by the imposition of agricultural cropping).Provided that a distinction is drawn between autogenicsuccessional progression under conditions of stable ver-tical structure (equivalent to Margalefs "main sequ-ence") and allogenic changes resulting from perturba-tions which cut across the true succession. It is possibleto accommodate both kinds of compositional changewithin a single explanative theory. If the overall ten-dency within pelagic ecosystems is towards a segrega-tion into an upper nutrient-limited, and a lower light-limited layer, as envisaged by Margalef (1978), then it isequally true that to a greater or lesser extent, wind-induced vertical mixing will override this segregation.As a result of the consequential integration of chemicalgradients, replenishment of nutrients in the trophogeniczone and redispersal of algal populations (cf. Reynolds1976b), the community may revert to a more primitivesuccessiona) stage.

3. The basic data and the method of Iheir analysis

3.1. Site data

The analysis is based upon 12 annual cycles of phytop-lankton standing crops (hereinafter referred to as"plankton-years") observed in four natural Englishlakes — Windermere (North Basin), Grasmere, CroseMere and Rostherne Mere - and two experimental en-closures ("Lund Tubes", A and B) installed in another- Blelham Tarn. Their geographical locations are shownin Fig. l.The series embraces a range of size, depth andretention time (shown in Tab. 1). Only Grasmere issignificantly flushed, but the plankton of Windermere issubject to dilution by high inflow discharges which alsoreplenish nutrient levels in the lake. Crose Mere andRostherne Mere are fed and maintained principally byphreatic supplies and, characteristically, they have longretention times and remarkably stable water levels. Un-

HOLARCTIC ECOLOGY 3:3 (1980)

510 _

Tab. 2. Chemical features of the lakes.

Fig. 1. The Iocalion of the lakes whose phytoplanktonperiodicity is described in this account. 'Lund Tubes' are in-stalled in Blelham Tarn.

der operational conditions, there is no significant inter-change of waters between the Lund Tubes and the Tarn(Lack and Lund 1974). More complete descriptions ofthe lakes appear in Macan (1970) and Reynolds(1979a).

Chemically, the series considered embraces soft- andhard-watered lakes, and a range of phosphorus availa-bility (see Tab. 2). Windermere and Grasmere are clas-sically oligotrophic lakes, occurring roughly in the mid-dle of Pearsall's (1921) classification (see also Macan1970, Jones 1972, Gorham et al. 1974, Pennington1978). In recent years, both lakes have been subject tomild enrichment, principally from increased dischargeof treated sewage, and are perhaps more convenientlydescribed as "mesotrophic". Crose Mere and Rostherne

Alkalinity(meq I"')

Max tot-P P-loading rate(g m"̂ ann"')

Windermerenorth) 0.20' 28^Grasmere 0.14' 33^RostherneMere 2.52^ >330' 0.7-2.8*Crose Mere . . . . 3.09-' >196^ 0.4-1.3'A(1977) 0.33* 42' 0.3 'A (1978) 0.77' 193^ 1.6'B (1976) - 106^ 0.4"B (1977) 0.36* 158^ 1.8'B (1978) 0.35* 260^ 2.4'

References: 1 - D. W. Suicliffe (pers. comm.) 2 - Unpubl.analytical data of J. Heron, E. Rigg, C. Woof. 3 -Reynolds (1979a) 4 - D. Livingstone (pers.comm.) 5 - Reynolds (1975) 6 - Author's un-published data. 7 - Reynolds and Butterwick(1979) 8 - J. W. G. Lund (pers. comm.).

Mere are naturally eutrophic calcareous lakes which arerelatively rich in phosphorus. Their epilimnia are liableto severe nitrogen depletion for long periods in summer(e.g. Grimshaw and Hudson 1970, Reynolds 1973a);indeed, nitrogen is more likely to limit phytoplanktonproduction than any other single nutrient, at least dur-ing summer (Reynolds 1979a).

Under operational conditions, the water Isolatedwithin the Lund Tubes is initially identical with that ofBlelham Tarn, which is also eutrophic, but soft-walered(Lund 1978a); it becomes progressively depleted ofnutrients, principally as a result of uptake by thephytoplankton (Lack and Lund 1974). Some experi-mental control of the chemical environment is achievedthrough the addition of inorganic fertilizers at the sur-face (e.g. Lund 1975). The schemes of fertilization Inthe plankton-years discussed below were as follows:Tube A was left unfertilized after isolation in March1977, but a significant loading of phosphorus (= 0.3 gP m'^) from the rich sediments at the bottom of the tubewas detected (Reynolds and Butterwick 1979; see alsoLund 1978b); for the 1976 experiment. Tube B wasisolated during the preceding winter, and was fertilized

Tab. 1. Morphometric features of the lake Basins.

Lake Area (ha) Max. depth (m) Mean depth (m) Retention lime (d)

Windermere (North Basin) 804.6' 64' 25.1' 270-370^Grasmere 64.4* 21,5' 7.7' 9-65'Rostherne Mere 48.7* 27.6* 13.3' 730*Crose Mere 15.2* 9.3* 4.8' 480-2590*Enclosure A, Blelham Tarn 0.16" 12.2« 11.3' °°'Enclosure B, Blelham Tarn 0,16 11.8* 11,1* =»'

References: I - Ramsbottom (1976) 2 - Macan (1970) and authors" recalculation, 3 - G, H, Hall (pers, comm,). 4 - Reynolds(1979a). 5 - Recalculated from dataof Pritchard (1961). 6-Harrison and Rogers (1977). 7 - Reynolds (1978a). 8 -Lack and Lund (1974). 9 - Under experimental conditions.

HOLARCTIC ECOLOGY 3:3 (1980) 143

once only (early May) with 3.0 kg potassium dihyd-rogen phosphate (equivalent to about 0.4 g P m"^);phosphorus, nitrogen (as sodium nitrate), silicate (assodium metasilicate) and chelated iron (ferric chloridedissolved with the molar equivalent of sodium ethylenediamine tetracetate) were added on a weekly basis toTube A (in 1978) and Tube B (in 1977 and 1978). inquantities calculated to restore the nutrient concentra-tions in the trophogenic layer (making due allowancefor the mixing depth) to arbitrarily predetermined levelsof 20 ng P, 300 ng N, 1000 ng SiOj and 100 ng total Feper liter.

The latter strategy was designed to mitigate the con-straint of possible nutrient stress on phytcplanktongrowth; algal bioassay of Tube B water in 1977(Reynolds and Butterwick 1979) indicated that thisprecondition was likely to have been satisfied. In 1978,the alkalinity of Tube A water was artificially raised, toa maximum of 1 meq I"', by the progressive addition ofpowdered calcium carbonate and sodium bicarbonateduring March and April.

3.2. Thermal structure

AH of these basins normally stratify in the summermonths (see Fig. 2) for the periods covered by thisstudy. The information for Windermere, Crose Mere,Rostherne Mere (1972 and 1973 only) and the LundTubes is drawn from weekly (or more frequent) temp-erature profiles measured in situ at the deepest point ofthe lakes with the thermistor circuit embodied in thecombined Mackereth probe (Mackereth 1964). Thedistribution of isotherms in several of these basins havebeen published previously (see Fig. 2 for references).Temperatures in Grasmere were routinely measured atselected depth stations only (Dr. J. G. Jones, pers.comm.) so that the diagram is based on less extensivedata. During 1971 only, temperatures in RostherneMere were measured with a mercury thermometer, in-serted into freshly collected Meyer-bottle samples(capacity about 1.5 1); the representation in Fig. 2 istherefore liable to some inaccuracy.

The shaded areas enclose the portions of each watercolumn in which the gradient of temperature changeagainst depth increments exceeded l°m~', and roughlycorrespond with the extent of the metalimnion. Theirhorizontal extent represents the period of thermalstratification while their vertical position and extentconveys the relative stability of the epilimnion.

Abrupt changes in the vertical extent of the epilimn-ion are codified at the top of each figure to distinguishphases of more stable 'microstratification' from periodsof more intensive wind-mixing and convectional coolingwhich resulted in the depression of the metalimneticsurface.

3.3. Phytoplankion data

Information on the biomass and species composition of

A78

• i i ' m ' i v ' V ' v i ' v i ' v i ' i x ' ~ x ' x r a i I n M IV V vivH VIIIX x XI xn

Fig. 2. Thermal stratification of the basins in the 12 "plankton-years" (Wn78 = Windermere Nonh Basin, 1978; Gr = Gras-mere, Cr = Crose Mere, Ro = Rostherne Mere, A, B = LundTubes A and B in BlelJiam Tarn). The shaded areas enclosethai portion of the water column wherein the gradient of letnp-erature vs depth is > I°C m"V The nearer the surface is ap-proached then the more stably stratified is the column. Thephases of stable stratification and epilimnetic deepening (as aresult of wind mixing and/or convectional cooling) are rep-resented at the top of each diagram by solid and hatched barsrespectively. The distribution of isotherms for Cr73 (Reynolds1976b), Cr74 (Reynolds 1976a), A, B77 (Reynolds & Butter-wick 1979) Ro72. 73 (Reynolds & Rogers 1976) and B76(Reynolds 1979b) have been published; Wn78, Gr78. A, B78and Ro71 are based on unpublished data.

the phytoplankton is based upon integrated water-column samples taken with a polyethylene hose (Lundand Tailing 1957). The vertical length of the columnswas 5 m, except those from Windermere (where a 7 mcolumn was used) and Rostherne Mere (4.5 m). A totalof 391 such samples cover the 12 plankton years; duringthe stratified periods, the frequency of sampling wasgenerally 1 week; Grasmere, Crose Mere and Rosth-erne Mere were sampled fortnightly in the winter; theLund Tubes were not routinely sampled during thewinter when they were open to the Tarn.

Aliquots of every column sample were fixed inLugol's Iodine on collection for later enumeration bythe sedimentation - inverted microscope technique(Lund et al. 1958). Smaller algae (< 20 \im) were

144 HOLARCTIC ECOLOGY 3;3 (1980)

1-

1-

1-

1-

1-

J 1 L

Wn78

A l l UrogI Cerot Tab

Gr78Ast t)inobSph As! Dinob As l *

OTQUr

Cr73Si.011 •

Crypt

Cr74 Cerat

A77Anab*

Asl Urog! Sph\ V \

A78- ^'if ./"'"'Ast*Crypf Ankf Frag*

i / y Stour

4 k /

Ro71 Cerat

20

10

Ast Anab

Ro72•10

AllEudo

Ro73 Mic

Sl.ost Eudo

B76Melo Aph Eud

\ I 1

B77

B78 Eud

lit IV V VI VII VIIIIX X XI xd I

-10

-1

IV V VI VII VIII IX X XI XII

Fig. 3. Fluctuations in the biomass of the algal standing crop present in integrated water column samples of 4.5-7.0 m verticallength (see text) for the 12 "plankton-years". Data are expressed in total algal cell volume (Rostherne Mere only) or chlorophyll aconcentration (all olher cases); units on vertical axes are in \i\ I"' or ng 1~' (xlO~^) respeclively. The algal species dominalingindividual peaks are identified by the following abbreviations: Anab, = Anabaena spp. (usually A. circinalis or A. flos-aquae)\Anky. = Ankyra judayi; Aph. = Aphanizomenon flos-aquae; Asl. = Asterionella formosa; Cerat. = Ceraiium hirundinella;Chrom. = Chromulina sp.; Crypt. = Cryptomonads (various, including/?/jo(/omo'!a5); Dinob, = Dinobryon (sp, undeiermined);Eudo. = Eudorina cf. elegans; Frag. = FragUaria crotonensis; Mic. = Microcystis aerugitwsa f. aeruginosa; Osc. = Oscillaloriaagardhii, (mostly v. isoihrix); Sph. = Sphaerocysiis schroeleri; Staur. = Siauraslrum spp. (various: see text); St. ast. =Siephanodiscus astraea; Tab. = Tabeilaria flocculosa; UrogI. = (Jroglerm americana; Volv. = Volvox aureus. The symbolsA . . . . A denole the period of Lund Tube closure in 1977 (both tubes were kept closed at the end of the 1978 season; Tube B wascontinuously closed between December 1975 and February 1977). The symbol V denotes Ihe single addition of phosphatenutrient to Tube B in 1976. The explanation of the solid and hatched horizontal bars a( the lop of each graph is noted in thecaption of Fig. 2, which also expands the titles of the individual plankton years. Chlorophyll data for Wn78 are presented with (hepermission of Dr. J. F. Tailing, F. R. S.

counted on a "Lund Cell" (Lund 1959). Some of theoriginal data have been published previously (for CroseMere, see Reynolds 1976a, b; for Rostherne Mere, seeReynolds 1978b; for Lund Tubes A and B in 1977 only,see Reynolds and Butterwick 1979) or are in prepara-tion by the author (Lund Tubes A and B in 1978). Theannual periodicity of aJgae in Windermere has beenpreviously described (Lund, in Macan 1970).

Estimates of chlorophyll a concentrations (uncor-rected for phaeopigments), calculated from spec-trophotometric absorption at 665 nm of extracts in 90%methanol according to the method of Tailing and Driver(1963), are available for all the samples except thosefrom Rostherne Mere. These data are presented in Fig.3. Biomass in Rostherne Mere is represented by totalcell volume, calculated from the product of the specific

HOLARCTIC ECOLOGY 3:3 (t980) 145

cell volumes of the individual species present and theirconcentration, estimated from direct counts (see be-low). Individual cell volumes were approximated fromdimensional measurements and geometric calculationsrelating to eel! shape (cf. Reynolds 1973b). The volumeof mucilage associated with colonial algae was ignored.Seasonal fluctuations in total cell volume in RostherneMere are also shown in Fig. 3, plotted to the scale 1 \ilr ' = 5 |ig chlorophyll a I"'. This arbitrary relationship isbased on the assumption that the dry content of algae isin the range 0.2-LO mg \i[~^, and that chlorophyll ac-counts for between 0.5 and 2.0% of the dry weight), butit will vary specifically and depending upon specificgrowth conditions.

Dominant (i.e. accounting for the largest proportionof the phytoplankton biomass) algae during periods ofhigh standing crops are also indicated in Fig. 3.

3.4. Community slructure and change: methods of analysis

The grouping of phytoplankton taxa into discrete as-semblages has been modelled on the standard sortingsystem employed by higher-plant ecologists inphytosociological analyses (e.g. Braun-Blanquet 1964).Each of the 391 sample counts was treated as a single"quadrat", or releve, ordinated in time rather than inspace. In every instance, the list of taxa (usually aspecies or, at least, a genus) registered by a countoscrewas analogized to presence in that relev6. As observedby Kalff and Knoechel (1978), the number of species tobe found in a given lake-water sample is partly a func-tion of the extent of search: as progressively larger vol-umes of water are examined, more species will inevita-bly be added. For the purposes of this analysis, whereabove all differences in community structure were beingsought, the use of the terms 'presence' and 'absence'required special definition. Here, 'presence' refers tooccurrence of algal cells in the smallest sample volumescanned in the original count (generally 1, occasionally10 mi). Thus, species occurring in concentrations of <0.1 ml"' were classed as 'absent'.

The 391 relev^s were initially grouped according totheir dominant species. Species lists in each of thesegroups were then further sorted for sub-dominantspecies having high coincidence both with the dominant,and with each other. The number of occasions that eachsub-dominant occurred with a given dominant wasnoted.

The next stage of the analysis attempted to refine thepreliminary groupings into labelled assemblages whichmight be representative of the species compositionduring any given stage of a plankton-year, yet still besensitive to changes in community structure. The pro-cess employed was a somewhat subjective one of 'trialand error', and the outcome was partly biassed by ear-lier observations (e.g. Reynolds 1973a, b, 1976a); nomathematical principle was invoked to determine theresult.

The third stage of the analysis required the introduc-tion of a quantitative expression of relative communitystability, which would also serve to identify the criticalperiods of structural change. The "succession rate in-dex" of Jassby and Goldman (1974), calculated directlyfrom the rates or change in the biomass of the speciespresent, is immediately applicable to ptanktonic com-munities. Lewis (1978a) argued convincingly that sincesuccession is a community phenomenon, the changes ina given species should be expressed in relation to theabundance of all the species in the community, and thatall individuals therein are equally weighted. He has thusproposed an alternative measure of succession rate(which he terms the "SD index": Lewis 1978a), inwhich all units in the population are accorded equalvalue, and the changes in each specific population affectthe whole community proportionately. The index isevaluated thus:

SD =

where bj (t) is the abundance of the i th species at time t,and B(t) is the size of the entire community.

In the present treatment, 1 have slightly modified theapplication of Lewis' Index to give a measure of what Iprefer to call the "rate of community change" since it issensitive to all major changes in community composi-tion, whether they are motivated as a consequence oftrue succession, or by any other non-directional process.Populations have been quantified in terms of cells, re-gardless of whether they are normally free living or col-onial. The abundance of each individual species presentwas equated with their populations (in cells ml"')counted in the standard water-column samples.

The modification 1 have embodied takes account ofthe fact that the volume of individual cells of differentspecies ranges over four to five orders of magnitude:weighting factors have been introduced in favour of thelargest cells which, at times, are dominant in spite ofyielding a low unit score. This is best demonstrated by asimple example.

Consider a hypothetical community consisting of 100Ceratium and 100 Rhodomonas cells ml"', which as aresult of typical growth of either species during the nextfive days, changes to 200 Ceratium and 800Rhodomonas ml"'. If the populations are scoredequally, then the rate of change yields the relativelyhigh value of 0.12 d"'. Yet at both stages the populationis clearly dominated by Ceratium, and the change in thecommunity structure is acutally small. To avoid suchparadoxical evaluations, I have scored 1 Ceraiium ml"'at the rate of 500 units; following similar reasoning,Stephanodiscus astraea cells have been accorded a valueof 10 units. These factors are somewhat arbitrary, butare designed to give unitary estimates comparable withsmaller-celled species which are potentially alternative

146 HOLARCnC ECOLOGY J:3 (1980)

Tab. 3. Summary of dominant species (D) and their mosi frequent associates (A) in 391 separate plankton samples (Relevis-n).

Dominant species (D) (n) Associated species (A)

1. DIATOMS1. Asierionella formosa

Asterionella formosa

2. Melosira ilalica

3. Stephanodiscus astraea

4. Fragilaria crotonensis

5. Tabellaria flocculosa var.aslerionelloides

(54)

(12)

(18)

(13)

(8)

(9)

6. Melosira granulata (2)

Cryptomonads (54), Ankislrodesmus (48), Chlorella (43), Melosira italica(39), Nitzschia spp. (35), Stephanodiscus astraea var. minutula (27), Cyclotellameneghiniana (23), Stephanodiscus hanlzschii (II), Fragilaria crotonensis (6),Tabellaria flocculosa (5).

Cryptomonads (12), Scenedesmus quadricauda (10), Stephanodiscus asiraea(10), Etakatothrix sp. (8), Fragilaria crotonensis {J), Stephanodiscus hantzschii(6).

Cryptomonads (18), Tabellaria flocculosa (18), Nitzschia spp. (18), Asieri-onella formosa (18), Fragilaria crotonensis (16), Cyclotella meneghiniana(15).

Cryptomonads (13, Asierionella formosa (13), Eudorina elegans (9), Stepha-nodiscus hantischii (8), Elakaiothrix (8), Fragilaria croionensis (8), Oocysiissp. (7).

Cryptomonads (8), Staurastrum pingue (8), Chlorella sp. (8).

Cryptomonads (9), Staurastrum cingulum (9), Ceratium hirundinella (9), Os-cillatoria agardhii (9), Gomphosphaeria naegeliana (8).

Cryptomonads (2), Ceratium (2), Fragilaria crotonensis {2) Asierionella for-mosa (2) Ctosierium aciculare (2), Siaurastrum cingulum (2).

II.7.

8.

9.

10.

11.

in.12.

13.

14.

CHLOROPHYTAEudorina elegans

Staurastrum pingue

Sphaerocystis schroeteri

Ankyra Judayi

Volvox spp.

CHRYSOPHYTADinobryon sp(p).

Urogtena americana

Chromulina sp.

(38)

(12)

(10)

(8)

(7)

(5)

(3)

(4)

IV. DINOFLAC3ELLATA15. Ceralium hirundinella

V. CRYPTOPHYTA16. Cryplomonas spp17. Rhodomonas minuta

Cryptomonads (38), Asterionella formosa (29), Oscillaloria agardhii (25),Fragilaria crotonensis {^i), Ankyra judayi (22).

Cryptomonads (12), Eudorina elegans (12), Fragilaria croionensis (12).

Cryptomonads (10), Asterionella formosa (8), Dinobryon sp. (6).

Cryptomonads (8), Eudorina elegans (1).

Cryptomonads (7), Eudorina elegans (7), Fragilaria croionensis (7), Pandori-na morum (7), Anabaena circinalis (4), Asierionella formosa (4).

Cryptomonads (5), Asterionella formosa (5), Tabellaria flocculosa (5), Chry-sochromulina (5). Mallomonas spp (5), Nuzschia sp. (4).

Cryptomonads (3), Asterionella formosa (3), Tabellaria flocculosa (3), Ma/-lomonas sp. (3), Dinobryon sp. (3).

Cryptomonads (4).

(34) Cryptomonads (34), Fragilaria crotonensis {21), Anabaena spp. (27), Micro-cystis aeruginosa (24), Closterium aciculare (18), Melosira granulata (17).

(50) (33), i4nAti(rod«mus (32), (Others < 25).

VI. CYANOBACTERIA18. Microcysiis aeruginosa .

19. Anabaena circinalis

20. Anabaena flos-aquae

21. Anabaena solitaria

22. Aphanizomenon flos-aquae

23. Oscillaloria agardhii (incls.

(53)

(22)

(2)(3)

(10)

(14)var. isoihrix)

(Exclusive 3) Cryptomonads (47),.4nfl6fltfna spp. (28), Ceratium hirundinella(27), Sphaerocystis schoeteri (18), Fragilaria crotonensis (10).Cryptomonads (20), Microcystis aeruginosa (12), Aphanizomenon flos-aquae(11), Fragilaria crotonensis (10), Sphaerocystis schroeteri (9), >4/ia6aenaflos-aquae (7).

Cryptomonads (2), A/iatae/ia circinalis (2), Aphanizomenon flos-aquae (2).

Cryptomonads (3), Anabaena circinalis (3), Anabaena flos-aquae (3).

Cryptomonads (10), Asierionella formosa (10), Anabaena circinalis (7), Mic-rocystis aeruginosa (7).

Siephanodisctts asiraea (6), Eudorina elegans (6).

HOLARCriC ECOLOGY 3:3 (1980) 147

dominants (e.g. 500 Ceratium = 250000 Microcystiscells; 1000 5. astraea cells = lOOOO Asterionella for-mosa cells). Trichomes oi Oscillatoria agardhii, in whichindividual cell walls are rendered difficult to identify inthe preparation for counting, are scored at the rate 1 ^mml"' = 1 unit. Applying the relevant correction to thesame hypothetical population, the modified index ofcommunity change becomes 0.002 d"'.

4. Phyloplankton species assemblages

4.1. Preliminary grouping of taxa

The initial phytosociological tabulation is not repro-duced here, but the preliminary grouping according tothe dominant species, together with their most frequentassociates, is summarized in Tab. 3. In this treatment•cryptomonads' includes a number of individual forms,variously ascribed to C. ovata Ehrenb., C erosa Ehrenb.and C curvata Guseva; Oscillatoria agardhii Gom. isnot distinguished from its variety isothrix Skuja.

Twenty-three species were recognized as dominants(D) during the twelve plankton-years considered. InTab. 3, sub-dominant species (A) are appended by thenumber of those relev^s in which they occurred. In gen-eral, the sub-dominants listed are the only ones whichoccurred in > 50% of these releves. Some species, how-ever, are included (e.g. Tabeilaria, Cyclotella spp.) be-cause they had a high coincidence with a stated domin-ant (e.g. Asterionella) of more cosmopolitan distribu-tion in only one or two of the plankton years, and so, onaggregate, were underscored.

Several consistent associations were identified (forinstance) among various diatom species and smallgreen algae, among the filamentous blue-green algae(Cyanobacteria), and among some of the largerChlorophytes. On the other hand, the cryptomonadgroup showed no clear association with any of the othertaxa: it occurred in 380 of the reieves, and was domin-ant in 50 of them. The analysis conceals possible specificdifferences (see above) and the fact that cryptomonadswere often relatively more numerous at times of diatomdominance.

In the lakes considered, there was a sharp separationamong the subdominant diatom species associated withvernal m3i\\m^ oi Asterionella formosa Hass., betweenthose occurring in the relatively poorer lakes (includingMelosira italica (Ehrenb.) Kutz. subsp. subarctica O.Mull., Cyclotella meneghiniana Kutz., Tabeilaria floc-culosa (Roth.) KiJtz. and the minutula (Kiitz.) Grun.variety of Stephanodiscus astraea (Ehrenb.) Grun.) andthe richer lakes {Siephanodiscus astraea s.s.); only Ste-phanodiscus hantzschii Grun. and Fragilaria croionensisKitton occurred in both series, and in the case of thelatter, there was an apparent separation between therod-shaped (in mesotrophic waters) and flared-endedforms (in the eutrophic lakes) recognized by Canter andJaworski (1978). The diatom populations which de-

veloped in summer, (dominated by Fragilaria crotonen-sis, Tabeilaria flocculosa or Melosira granulata(Ehrenb.) Ralfs), differ significantly from the vernalpopulations in the relative paucity of associated diatomspecies: instead, the most common associates includesuch 'cosmopolitan' desmid species as Staurastrum pin-gue Teiling,5. cingulum (W, et G. S. West) G. M. Smithand Closterium aciculare T. West var. subpronum W. &G. S. West, together with elements of the summerplankton {Ceraiium hirundinella O. F. Mull, Gomphos-phaeria naegeliana (Unger.) Lemm.).

Ceratium represents the major algal biomass in someof the basins. In Rostherne Mere, it often plays a secon-dary role to Microcystis, but it does dominate in certainyears. These two algae may occupy a similar position inthe seasonal succession, and dominance may be decidedby the outcome of competitive interaction (for a morecomplete discussion, see Reynolds 1978b). Undersuitable conditions (as yet undefined), Microcystisaeruginosa Kutz. emend. Elenkin may occur virtually tothe exclusion of all other taxa, as was observed inRostherne Mere, and in Tube B during both 1976 and1978. Species of Anabaena and Aphanizomenon fre-quently occurred together, but Oscillatoria, which inthis analysis achieved its best growth in autumn, standsapart.

4.2. Assemblage determination and lahels

Algal species which showed a high frequency of conci-dent presence in the releves were grouped together as"assemblages'. Fourteen such assemblages were eventu-ally recognized, and their main representatives arelisted in Tab. 4. Each is identified by a label, but it isimportant to stress that the use of a particular label neednot indicate which species is dominant. For this reason,the use of non-specific labels is preferable (I have re-sorted to alphanumerics); the labels are preserved in thetext, however, to aid clarity. For example, a populationdesignated ""^Asterionella/Melosira italica" (group ( l j ) ,might be recognized by dominance of just one of thesespecies, together with others in the assemblage, evenwhen the other is absent; in the same way, a populationdominated by a Mallomonas species, would be ascribedto the "Uroglena/Dinobryon" group [5]

The first assemblage [1] represents the vernal popu-lations in Windermere, Grasmere and Blelham Tarnisolated in the Lund Tubes: Asterionella formosa,Melosira italica and Cyclotella spp were variouslyprominent, with such typical sub-dominants as Tabei-laria, Nitzschia, and smaller Stephanodiscus spp, as wellas Chlorella, Ankistrodesmus and cryptomonads. Group[2] ts the analogous assemblage typical for Crose Mereand Rostherne Mere, in which either A. formosa, Ste-phanodiscus astraea (s.s.), S. hantzschii or (more rarely)Fragilaria crotonensis was dominant over the others andwhere cryptomonads and green algae (e.g. Scenedes-

148 HOLARCnC ECOLOGY 3:3 (1980)

Tab. 4. The algal assemblages.

Group Main codominants

1. Asterionella/Meiosira italica

2. Asterionella/Stephanodiscus astraea

3. Eudorina/Volvox

4. Sphaerocystis

5. Uroglena/Dinobryon

6. Anabaena/Aphanizomenon

7. Tabeilaria/Fragilaria/Slaurastrum

8. Melosira granulaia/Fragilaria/Closterium

9. Microcystis

10. Ceraiium

11. Pediastrum /Coelaslrum

12. Oscillatoria

Communities of uncertain statusX. Opportunists (e.g. Ankyra,

ChromuUna)Y. Cryptomonads

Cyclotelta spp., Nitzschia spp. Chloretla, Ankistrodesmus, Cryptomonads

Fragilaria crotonensis, Stephanodiscus hantzschii, Scenedesmus, Elakatothrix,Oocystis, Cryptomonads

Pandorina, Anabaena, Aphanizomenon, Cryptomonads, Ankyra

Asterionella, Dinobryon, Uroglena, Anabaena, Cryptomonads

Mallomonas, Chrysochromulina, Asterionella, Tabeilaria

Microcystis, Cryptomonads

Ceratium, Gomphosphaeria, Cryptomonads

Microcystis, Ceratium, Closterium, Slaurastrum, Cryptomonads

Ceratium, Fragilaria, Anabaena, Cryplomonads

Fragilaria, Microcystis, Cryptomonads

Dictyosphaerium

Asterionella, Cryptomonads

mar, Elakatothrix, Oocystis or Tetrastrum spp.) may bemajor sub-dominants (cf. Reynolds 1978a). Summerdiatom-dominated assemblages were distinguishablefrom the vernal crops: in Crose Mere, they were typifiedby populations of Melosira granulata and/or Fragilariacrotonensis with (occasionally) A. formosa (seeReynolds 1973b) and (more frequently) desmids be-longing to the genus Closterium (group [8]); the corres-ponding assemblage in the Lake District waters (group[7]) is represented by F. crotonensis, T. flocculosa and(at least in Grasmere) A. formosa, with various speciesof Staurastrum sub- or co-dominating. These groupingstherefore take account of the evident polarization, be-tween vernal [1, 2] and summer [7, 8] populations andbetween the relatively poorer [1, 7] and richer [2, 8]lakes.

Green algae were dominant in several of theplankton-years shortly after the diatom phase. Popula-tions in which Eudorina or Volvox spp. are apparentlyclosely allied, are grouped together as assemblages [3].In Windermere, Grasmere and A 1977, Sphaerocystisschroeteri Chod. was the most prominent green alga,often occurring with different sub-dominant species;such populations [group 4] may thus be distinguishedfrom the preceeding group [3]. The chrysophyte-domi-nated populations, shown in Tab. 3, share obvious af-finities and are accordingly grouped as assemblage [5].It may be closely allied with [4], but in the absence ofsufficient supporting evidence, the taxonomic distinc-tion is preserved. Groups [3], [4] and [5] are viewed asalternative assemblages associated with the early stagesof thermal stratification in lakes.

The heterocystous cyanobacteria {Anabaena,Aphanizomenon) constitute another well-defined as-semblage [6]. Besides being mutually alternative do-minant and co-dominants in different communities,these genera share many common features of mor-phology, biochemistry and ecology (cf. Reynolds1973a). These algae frequently succeeded dominantEudorina-Volvox populations, or occasionally replacedthem in the periodic sequence.

Populations dominated by Microcystis were suffi-ciently distinct to merit separate recognition (as group[9]). The assemblage should possibly include Ceratium-dominated populations, since their ecological rangesundoubtedly overlap, but other differences between therespective populations that they came to dominate soeffectively warrant the present separation of the Cera-tium assemblage [10].

The Pediastrum-Coeiastrum group [11] was neverclearly dominant in any of the plankton years, but itconstituted a distinctive sociological element in theeutrophic meres, where it was more strongly rep-resented in spring and autumn pulses (see also Reynolds1973a).

Dominance by Oscillatoria usually occurred duringwinter, but was observed occassionally in summer(especially in the Lund Tubes) in the interludes ofminimal biomass (see Fig. 3) between maxima of otherassemblages. In spite of this apparent 'dominance bydefault', Oscillatoria populations often showed distinc-tive periodicties and specialized survival mechanisms,compared with their competitors. They are thus af-forded assemblage status [12].

HOLARCTIC ECOLOGY 3;3 (1980) 149

The two remaining groupings are not readily ab-sorbed into this classification. The smaller algae(nanopiankton, or n-algae), exemplified in the presentanalysis by Ankyra judayi; (G. M. Smith) Fott (in TubeA, 1978) and by Chromulina sp. (Tube B, 1978), andcharacterized by ephemeral bursts of rapid growth cul-minating in short-lived maxima, occupy the role ofopportunist species. These are referred to as group [X].It may also have some affinity with the Eudorina-Volvox group [3]. The cryptomonads, which are presentin all of the other assemblages, constitute the finalcategory [group Y].

5. Rates of community change

Periodic changes in community structure in each of thetwelve plankton-years is illustrated in Fig. 4. Theserepresentations identify the phases of more rapidstructural change as peaks, usually exceeding a rate ofchange equivalent to 0.1 d"'. The tendency to skewness(usually to the left) indicates that the onset of change istypically abrupt, but the rate of change weakens as onespecies becomes dominant over its competitors. Itshould also be noted that the rate of change was gener-ally lowest during the vernal, prestratified phase (whendiatoms were usually dominant) and during the tale

CM-

CM-

OI-

J L

Wn7812

Cr73 :Y : 2

• 3 : 6

8: 10 :8ia/Y

A77

A 78 nYl 6-712

' v i ' v i i ' v i l l ' IX ' X '

Ro7112,

^ .̂g^k '̂2 i6|X)i 10

-0-1

Ro72 i3•OI

Ro73

12 12•0-1

B76

B77 0-2

O2

I II til IV V ' v i ' v i i ' v i l l ' IX ' X 'x i ' V I ' V I I ' V I H ' ly 'I ' M ' III ' I V ' V ' V I ' V I I ' V I H ' ly ' X ' x i XII

Fig. 4. The rates ofcommunily change in eachof I he 12 plankton-years,measured from thepopulation present inintegrated column overperiods of 3-28 d by theLewis (1978a) SD indexwith minor modificalions toscoring (see text). Veriicaiscale is in rale of changed̂ V Vertical broken linesindicate changes ofdominance from oneassemblage type to another,identified by the digiialnotations (1-12. X. Y) givenin Tab. 4. The explanationof the solid and hatchedbars at the top of eachgroup is given in the captionto Fig. 2; other symbols areas in Fig. 3.

150 HOLARCTIC ECOLOGY 3:3 (1980)

phases of stratification (at least in the richer lakes) onceMicrocystis-[9] or Cerarmm-dominated populations[10] had established dominance.

Empirical solutions for shorter time intervals (3-7 d)afford better resolution of the points and rates of com-munity change than do those for the longer intervals(14-28 d). Thus, the peaks are not always comparablebetween the various plankton-years. Here, their princi-pal value lies in identifying the intermediate periods ofslow rates of change, when the structure of the com-munity is more stable, one or more species being clearlydominant. The application of alphanumeric notations(see Fig. 4) to summarize the composition of thephytoplankton during these phases of relative com-munity stability permit the periodicity of each plankton-year to be viewed in terms of the sequence of dominantassemblages. Moreover, comparisons between differentlakes and different years are considerably simplified.

In view of the assertion advanced at the outset (seeSect. 1) that phytoplankton community structure maybe particularly sensitive to changes in physical stability,it is pertinent to draw attention to the fact that only halfof the recorded changes in community structureobviously coincided with alterations in physical stability(represented in Figs 2—4 by solid and hatched horizontalbars). Of the 82 community transitions identified in Fig.4, 21 can be directly related to the onset of more stablystratified conditions, and a further 19 follow phases ofincreased mixing and epilimnetic deepening. The mostconsistent response throughout the series of plankton-years is the replacement of vernal diatom-dominatedassemblages [1,2] after the initial onset of stratification.The response is most rapid in the smaller basins (in-cluding the Lund Tubes) where it occurs within a fewdays, less so in the larger basins (like Windermere and,to a limited extent, Rostherne Mere). Stratificationfavours the ascendancy of the Eudorina-Volvox as-semblage [3] in the more eutrophic waters, and theSphaerocystis [4] or Chrysophyte [5] assemblages in thepoorer lakes. The Anahaena-Aphanizomenon as-semblage [6] apparently occupies an intermediate posi-tion, either succeeding [3] in the more fertile systems, ordominating in its absence. In Lund Tube A, 1977, Ana-baena spp. co-dominated with Sphaerocystis schroeteri.

The desmid-diatom communities [7, 8] frequently(though not always) developed following periods ofmore vigorous wind-mixing and epilimnetic deepening.The assemblages remained dominant only if the mixingwas sustained (as in Windermere and Tube B, 1977),and hence tended to be more prominent towards theend of the summer. In the shallower lakes (e.g. Gra-mere, Crose Mere), they also survived well after de-stratification, but Oscillatoria, cryptomonads or evenwinter diatom assemblages [1, 2] frequently becameestablished in the deeper basins, albeit in low concent-rations.

In earlier considerations of the phytoplanktonperiodicity of Crose Mere (Reynolds 1976a, b, c) it has

been shown that if the wind-mixing that enlarges theepilimnetic volume in summer is not sustained, ascen-dent diatom populations may be rapidly replaced byassemblages representing earlier successiona! stages. Asimilar effect was found in Grasmere, with the re-estah-lishment of a Dinobryon-dominaied assemblage [5]. Inother instances, there was a more or less rapid progres-sion to dominance by Microcystis or Ceratium popula-tions. The significance of this response is not entirelyclear. In each case, populations of one or other of thesealgae had been slowly increasing prior to the disturbedphase. Both algae are able to regulate their position instratified water columns (Reynolds and Walsby 1975,Heaney 1976), whilst other features of their biologyseem to be well-adapted to survival in strongly segre-gated environments (sensu Margalef 1978). That theydo not become dominant earlier in the year is partly afunction of their relatively low rates of growth, but mayalso be infiuenced by competition from species whichmay be better adapted to the conditions initiallyobtaining after stratification. Whether or not either iseventually destined to become dominant, without theintervention of wind mixing cannot be resolved on thepresent evidence, although the earlier ascendency ofeither species in Rostherne Mere is not conclusivelycorrelated with either markedly stable or unstablephases. Once established however, these assemblageswere able to survive subsequent alternations in thermalstructure, at least while the columns remained stratified.Resistance to such loss control mechanisms as death,sinking and grazing may be especially advantageouswithin this context. Thus, Microcystis and Ceratiumconceivably represent the climatic stage of the seasonalsuccession in the plankton years considered, at leastduring the stratified period.

Nineteen of the observed transitions indicated in Fig.4 which were not obviously correlated with alternationsbetween turbulent and calmer phases occurred in theprestratified period. For the most part, these representeither the change from low winter populations domi-nated typically by cryptomonads, to the vernal popula-tions in which diatom assemblages [1, 2] predominate,or to a phase where the assemblages are co-dominant,or to a post-maximal diatom phase, when cryptomonadsare again relatively more abundant. It may be post-ulated that these transitions are regulated by the am-bient light climate in mixed columns (cf. Tailing 1971),and possibly compounded, at least in the mesotrophicsystems, by the effects of nutrient depletion.

The remaining 23 transitions all occurred through thesummer and autumn and independently of alternationsin physical stability. These include a number of exam-ples of sequences common to several separate plankton-years: for instance, from the chrysophyte [5] to theSphaerocystis-assemh\agc [4[ in Grasmere and A 1977(the sequence was reversed in Windermere), and fromEudorina-Volvox [3] \o Anabaena-Aphanizomenon [6]in Crose Mere (twice), and Rostherne Mere (1973

HOLARCriC ECOLOGY 3:3 (1980) 151

only). The replacement of Eudorina by Anabaena orAphanizomenon as the dominant alga in Crose Merehas been shown to be directly associated with epilimne-tic depletion of supplies of combined nitrogen(Reynolds 1976b), and It is arguable that such progres-sive changes are symptomatic of stable, physical seg-regation as envisaged by Margalef (1978). Severaltransitions were directly consequential upon the rapidelimination of populations of smaller algae {Ankyra,Chromulina [X]), in which grazing by zooplankton wasprobably a major factor (unpubl. data). In spite of fre-quent fertilization of the tube systems, Eudorina popu-lations were also subject to collapse, accompanied byprolific sexual reproduction possibly stimulated by theonset of adverse conditions (e.g. pH: see Reynolds andButterwick 1979). Equally, a phase of rapid growthfollowed by rapid attrition of vegetative populationsmay represent a discrete survival strategy for these al-gae. Another type of transition which was observed onlyin the fertilized tubes (B1977, A1978) was the survivalof low biomasses (cf. Fig. 2) of Oscillatoria or cryp-tomonad populations following the collapse of domin-ant Eudorina populations: this temporary 'defaultdominance' (see Sect. 4.2.) probably has no special re-levance to the controlled succession from one majorbiomass peak to the next. Finally, attention may bedrawn to the ascendancy of Eudorina in Tube B, in1976, shortly after heavy fertilization with phosphate inMay: its growth appears to have been a tangible re-sponse to the increased availability of nutrients.

X, 3 6 4 5 9 X, 10 8 11 7 2 12 1 Y

B- - -

-•

--

-

- B - -—

-

•

-10

-20

Q L-30

64Fig. 5. TTie ranges of mixed column-depths obiaining duringdominance or co-dominance by the phyioplankton as-semblages (1-12, X, V, identified in Tab. 4) in the 12plankton-years. The occasions when rhe various assemblageswere dominant are shown in Fig. 4; corresponding mixed-column depths are drawn from Fig. 2. Data for Chromuli-na-{X,) and /4nAvfl-(X;) dominated assemblages are pre-sented separately. The vertical bars are arranged in ascendingorder of their mean values. Assemblage ] 1 was co-domlnanionly in the fully mixed column of one lake (Crose Mere).

6. The mechanisms of periodicity: succession, shiftand reversion

The foregoing analysis of periodicity suggests that rec-ognizable alga! assemblages are broadly characteristicof potentially quantifiable features of the physical andchemical environment which they inhabit, and that thetransitions between them may be classified according towhether or not they occur in response to changes in thephysical environment. In this section, I wish to refinethese criteria sufficiently to propose a generalizedmodel accommodating periodic changes.

Fig. 5 summarizes the ranges of epilimnetic or fullisothermal mixed depths obtaining during the periodswhen the various assemblages were dominant, and isbased directly upon the information presented in Figs 2(mixed depth) and 4 (periods of assemblage domi-nance). The assemblages are arranged in ascendingorder of their mean values. Thus, progressively deepermixing of the column is likely to favour the dominanceof assemblages towards the right hand side of the dia-gram; column stability should tend to select those to-wards the left. The obvious overlaps of range confirmthat mixed depth alone is not the factor determiningwhich of the assemblages will be dominant, but ratherthat it interacts with other environmental factors (e.g.

light penetration, mean temperature, vertical distribu-tion of nutrients) and the specific adaptations of thealgae concerned. However, il has already been shownthat many of the assemblages sharing similar mixeddepth ranges segregate between the chemically richerand poorer waters, and that where these assemblages dooccur in the same lake, their periodicities may be re-lated to progressive nutrient depletion. In this way,sustained mixing or stability is likely to select one of alimited number of individual assemblages whose com-petitive advantage may eventually be resolved by theavailability of critical nutrients. So long as the physicalconditions remain relatively constant, the availabilityand distribution of resources, particularly of nutrients,will be more or less altered by algal growth, perhaps tothe point where representatives from another as-semblage are favoured. Indeed, this is likely to be themajor factor contributing to autogenic successionalchanges in the composition of the community (cf. Mar-galef 1978).

Environmental perturbations which change thestructure of the physical environment and, to a varyingextent, recharge^epilimnetic nutrient availability, cutacross the direction of these autogenic changes. Round(1971) aptly described such perturbations "shockperiods"; potentially, they are conducive to the rapid

152 HOtJ^RCTlC ECOLOOY 3:3 (1980)

Gr78

Wn78

A77

Cr73

Cr74

Ro71

10 ^'-•7 -12

-8*10

2—*-6

Ro72

Ro73

B76

B78

A78

B77

9' • •7

Fig. 6. Simple 'flow diagrams' illustrating the periodic changes in dominance by the various assemblages (identified in Tab. 4)during the 12 plankton-years. Horizontal arrows indicate transitions which are not associated with changes in thermal stability;interludes of epilimnetic deepening (see Fig. 2) are shown by the vertical offsets in the fiow lines, leading to the next dominatingassemblage(s). The single addition of phosphate fertilizer to Lund Tube B in 1976 is represented by the break in flow, F. Phases ofdominance by the Oscillaloria (during the stratified periods only) and the ciyptomonad assemblages (throughout) are omitted (seetext).

eclipse of pre-existing populations by representatives ofassemblages better adapted to growth under the newconditions obtaining.

Both kinds of community change are represented inFig. 6, in which the sequence of dominant assemblagesobserved in each of the plankton-years is plotted as asimple flow line. In each case, the horizontal arrowscorrespond with autogenic transitions which occurredindependently of major changes in physical stability(examples shown include those from Eudorina [3] toAnabaena/Aphanizomenon [6] and from Chrysophytes[5] to Sphaerocystis [4], discussed earlier); transitionsdirectly following interludes of epilimnectic deepeningare indicated by the vertical offsets (frequently leadingto dominance by summer diatom assemblages [7, 8].

Ensuing transitions can be of either kind. Continua-tion or extension of vertical mixing may favour the per-sistence of summer diatom assemblages [7, 8], as inGrasmere, Crose Mere and, in certain years, in the ex-perimental enclosures, or their eventual replacement byOscillatoria-dominaled populations, as occurred in au-tumn in Windermere and Rostherne Mere (1973). Ipropose to distinguish such responses to changed physi-cal structure by referring to them as 'shifts'. Alterna-tively renewed physical stability may lead to a partial

re-capitulation of an earlier sequence (such as the re-placement of the diatom-dominated assemblage [7] byChrysophytes [5] in Grasmere, or the reestablishmentof the Eudorina- Volvox assemblage [3] after domi-nance by Anabaena or Aphanizonomen [6] in CroseMere). In other words, the sequence reverts to an ear-lier successional stage. The single fertilization of LundTube B in 1976 (represented by the offset labelled 'F' inFig. 6), which led to dominance by Eudorina, is analog-ous to reversions consequent upon the increase in avail-able nutrients (initially introduced by the entrainmentof hypolimnetic water) and the subsequent re-stratifi-cation of the epilimnion (e.g. Reynolds 1976a, b).

It is uncertain whether the ascendancy of the Mic-rocystis [9] - and Ceratium [10] populations is the resultof shift or of reversion. The possibility that either mighthave appeared without the intervention of increasedmixing has already been discussed. What is apparent,however, that once established, populations of both al-gae seem capable of surviving alternations in physicalstability, at least whilst stratification persists. Evidently,these algae are adaptable to a wider spectrum of en-vironmental fluctuations than many of their com-petitors.

The sequences of the major algal assemblages illus-

tl HOLARCTIC ECOLOGY 3:3 (1980) 153

trated by the 12 plank ton-years can thus be resolved interms of their particular environmental requirementsand the capacity of changing physico-chemical condi-tions to meet them. The community responses can beclassified into three categories:(a) true autogenic succession (the 'main sequence' of

Margalef 1978), under relatively constant physicalconditions, permitting structural segregation;

(b) allogenic5/u/M, arising from more pertnanent vari-ations in physical structure;

(c) reversions, arising from temporary structural per-turbations, followed by renewed thermal stability.

Just as the physical characteristics of the environmentdetermine the direction of phytoplankton periodicity,then chemical characters will influence both the rate ofprogression, and the staning point of the sequence. Ifthis is indeed the case, then it is possible to formulatesome general model to account for the sequencesobserved in the twelve examples considered here, andwhich may be applicable to many other lakes. To thisend, a "possibility matrix" (Fig. 7) is advanced. Its axesare physical stability of the medium and the generalavailability of (unspecified) limiting nutrients. Thematrix is divided into areas labelled according to thealgal assemblage most likely to be dominant at thoseco-ordinates. The evaluation of the axes is clearly pre-mature, owing to differences in specific limiting nut-rients among the given lakes and the fact that the effectsof column mixing will be conditioned by light penetra-tion and day length (it might be more desirable to labelthe mixing axis in terms of optical depth of the mixedlayer, but I prefer to avoid the introduction of anotherconcept at this stage of the argument). It must also bestressed that boundaries between the assemblages aretentative, and that the linear delimitations representrather wider critical boundaries (which are not,moreover, necessarily straight lines). A boundary be-tween the areas of assemblages [9] and [10] has beendeliberately omitted since in some lakes they may wellrepresent direct alternatives (Reynolds 1978b). As-semblages [12] and [Y] are also omitted for simplicity:on current evidence they might both conceivably occupymost of the area of the matrix.

The arrangement of assemblages is based upon theiroccurrence in the 12 plankton-years. For example, theEudorina-Volvox [3] and opportunist groups [X]occupy the area of strong thermal stability and abun-dant nutrients. The Chrysophyte assemblage [5] extendsover a range of mixing in the area of high nutrient stress.The diatom assemblages [7, 8] are located towards thebottom of the matrix (welt-mixed systems), while thevernal diatom populations (1, 2) are located in the areaof complete (or nearly so) mixing.

The lower part of Fig. 7 shows the directions of thethree types of periodic progression through the matrix.Following the onset of stable thermal stratification (lowcolumn mixing), the co-ordinaies of a starting point areestablished towards the top of the matrix. The position

NUTRIENT AVAILABILITY

high iowlow"!

low highJ'"?z

lowNUTRIENF STRESS

SUCCESSION

SHIFT

Fig. 7. A hypothetical "possibility matrix" showing the mostlikely dominant algal assemblage (codified as in Tab. 4) as-sociated with co-ordinates determined in terms of general re-lative availability of (unspecified) limiting nutrients and col-umn ml.xing. The direction of periodic progressions from onedominant assemblage to the next is represented in the lowerpart of the figure: autogenic successional changes are rep-resented by rightward horizontal progression: environmentalperturbations wrought (e.g.) by wind-mixing normally result ina downward progression through the matrix, with some left-ward drift. If mixing persists, a rightward direction is resumedto give a new sequence (shift); re-establishment of stablestratification determines an upward direction, representing re-version. Usage of the terms "succession", "shift" and "rever-sion" is defined in the texi.

on the horizontal axis is determined by the availabilityof nutrients. The time course of subsequent environ-mental changes is then tracked through the matrix, topredict the dominant algal assemblage. The directionand the rate of progression will thus express the re-S(X)nse or the phytoplankton community to changes inthese two major environmental characteristics.

Generally, the 12 periodicity sequences consideredare accommodated in this scheme. There are detailweaknesses (e.g. the directionality of the [4]-[5] trans-ition in the mesotrophic systems), but they may beovercome if the stringency of the boundaries is relaxedslightly. In any case, more data from more lakes arenecessary to impart the degree of resolution required

154 HOLARCTIC ECOLOOY 3:3 (1980)

Tab. 5. Growth and survival strategies for representative species of the algal assemblages.

Assemblage Physical growth Critical factors governingTypical Major factors con- Survival mecha- Perennationpreferences onset of growth growth rates trolling growth nisms

1. Asterionella' Well mixed. Light climate. Low* Stratification.Meiosira ilalica Tolerant of win- Low-moderate P {< 20 (k = Phosphorus,

icr temperatures [igl~'). 0.05-0.1). Silica.(4-6''C). Parasitism.

Increased sinking Maintenance ofrate. low vegetative

stocks.Meiosira has re-sting stages.

2. Aslerionelia- Well mixed. Light climate. Low- Light.Stephanodiscus Tolerant of win- Moderate-High P (> 20 Moderate* Stratification.astraea ter temperatures ng I"'). (k = Silica.

(4-6*C). Silica > 0.2 mg I-'. 0.1-0.2). Parasitism.

Increased sinking Maintenance ofrates. low vegetative

stocks.Stephanodiscushas possible re-sting stages.

3. Eudorina- Stratified columnsNutrients (especially N) HighVolvox (Epilimnia < 10 moderate to high. (k =

m). Long day (> 12 h). 0.4-0.7).Temperatures > SX.

Mixing.Nitrogen, phospho-rus.Parasitism.Grazing?High pH?

Rapid growth Spore survival onfollowed by sex- sediments,ually reproducedspores.

4. Sphaerocysiis ± Stratified co-lumns

Nutrients; moderate Moderate(0.2-0.5).

Nutrients.Parasitism.Competition.Grazing.

Slow attrition. Unknown.

5. Chrysophytes Stratified columnsNutrients: low - Low -moderate (Tolerant of moderate (klowP). - 0.1-0.4).

Competition.Nutrients.Parasitism.Mixing?Grazing.

Sporulation. Spore survival onsediments.

6. Anabaena- ± Stratified co-Aphanizomenon lumns.

Temperatures

Light climate: day length Low -may be as important as moderate (ktotal insolation. = 0.1-0.5).Nutrients (esp. P) mod.- high, but tolerant oflow N.

Phosphorus.Bloom formation.Parasitism.Protozoan grazing.

Low attrition du- Spores survive onring growth. sediment.Akineie forma-tion.

7. Tabellaria/ Increased mixing Free nutrients: moderate Moderate - Free nutrients? Si,Fragilaria/ and release of - high, including high Fe, N.Staurastrum free nutrients in available iron. (k = Thermal stability,

epilimnion. 0.2-0.6). Grazing?

Increased sinking Maintenance ofrate. low vegetative

stock. Survival ofsediments may beprolonged.

8. Meiosiragranulata/Fragi-laria/Closterium.

Increased mixing Free nutrients: moderate Highand release of - high, including (k =free nutrients in available iron. 0.3-O.6).epilimnion

Tliermal stability. Increased sinking Maintenance ofNutrient availability rate. low vegetativeesp. Fe, Si, N. stocks. M. gra-Grazing? nulata has pro-

longed survivalon sediments.

9. Microcystis Persistent or Inoculation? Lowstable stratifica- Hypolimnetic anoxia. (k < 0.2).

' tion Long day length but lowlight intensity.Temperature > H X .

Nitrogen, phospho- Low loss rates. Maintenance ofrus. Compensatory vegetative stockAutumnal destratifi- bouyancy regula- on sediments,cation Bloom forma- tion.tion.

10. Ceratium Stratification. Persistent or intense Lowsegregation of ecosystem (k < 0.2).structure.

Competition. Low loss rates.Nutrient availability Compensatorywithin aerated layers, migratory beha-

viour.Encystment.

Cysts on sedi-ment.

11. Pediastrum/Coelastrum

Unstable High nutrientenriched water concentrations,columns. Simple organic

substrates?

Potentiallyhigh?

Nutrient depletion.Parasitism?

Prolonged vege-tative survival onsediments?

I I ' HOLARCTIC ECOLOGY 3:3 (1980) 155

12. Oscillatoriaagardhii

Mixed columns.low averageillumination.

LackLow

of competition.washout.

Apparentlylow(k =0.02-0.04).

Competition.Washout.Parasitism.Photo-oxidation.

Algal stratifica-tion.

Maintenance ofvegetative stocksin water columnsor on sediments.

X. "Opportunists" Stratifiedcolumns?

Abundant free nutrients. HighTemperatures > 8°C. (k =

0.5-0.8).

Nutrient limitation.Grazing?

Facultative rapid Unknown,growih. Possibly resting

spores.

Y. Cryptomonads Various:possiblespecificpreferences.

Light climate.Low grazing pressure.

Moderate? Grazing. Wide tolerance Maintenance of(k = gene- Nutrient limitation, range of envi- vegetative stocks,rally < O.S). Light climate. ronmental condi-

tions.

• Under the prevailing temperature conditions at the times these algae develop, these rates exceed those of most of (heir competitors, andare in fact relatively high.

for a wholly predictive matrix. Fig. 7 is intended to pro-vide a conceptual framework against which the seasonalperiodicity of phytoplankton in all stratifying lake sys-tems might be assessed.

7. Phyloplanklon growth and survival strategies

It is implicit that the mechanisms regulating periodicityare closely dependent upon significantly differentadaptations for pelagic life among the algae themselves.Of the species available at a given time, the likely do-minant will be the one which is best suited to exploit thecontemporary environmental conditions. In fact, thiswill not always be the case. Biotic factors (involvingherbivorous animals and parasites) and the capacity forvegetative survival of preceeding dominants are obviouscomplicating factors, with the result that the dominant isnot necessarily the best adapted on theoretical grounds.Conversely, biological suitability is not a guarantee ofecological success, but the range of possibilities in com-munity composition is reduced, at least, to the extentwhere periodic assemblage changes are broadly pre-dictable.

How well do the transitions between assemblagesrepresented in the matrix coincide with our currentknowledge of specific survival strategies and to whatextent do they enhance that knowledge? Factors whichwere possibly critical to the initiation and limitation ofgrowth of each of the 14 assemblages, together withbiological features relevant to their survival, are shownin Tab. 5. The information presented is derived princi-pally from the 12 plankton-years considered, but it issupported by additional observations made in the samelakes at other times. The growth rate values cited (k, inIn units d"') are, in most cases, net increase rates, andapply only to algae dominating the assemblage. Thesuggested mechanisms for survival and perennation alsoapply only to dominant species.

Nevertheless, the available information largely com-plements the species periodicity (Fig. 4). For example, itis possible to propose that Ihe respective capacities of

some diatoms to grow well at low temperatures, ofEudorina to develop large populations in warm, stablenutrient-rich epilimnia and of Microcysiis to maintainits slowly elaborated population in suspension throughsummer, determine the response of the phytoplanktoncommunity to the broad annual cycle of environmentalchanges in eutrophic lakes. However, it is dangerous toassume that the behaviour deduced for specificorganisms is necessarily the best that they could possiblyhave achieved under different conditions. In otherwords, doubt remains as to whether the observed fea-tures of growth and survival determine the communityresponse to changing environmental conditions, orwhether they are to some extent its consequence. This isa field in which further experimental evidence is re-quired.

It is emphasised that these interpretations are con-fined to the periodicity of the assemblages. Whereas it ispossible to suggest the causal mechanisms for sometypical sequences observed (for instance, [2] —> [3] —*[6]), 1 have not attempted to account for the selection ofthe dominant species within each assemblage. In theexample given, the dominants in the sequence could aseasily be [Stephanodiscus] —* [Eudorina] -*[Anabaena]as [Asterionella] —* [yolvox] —* [Aphanizomenon] or asany permutation of species representative of these as-semblages).

The outcome of within-assemblage competition isbeyond the scope of the present treatment. With theexception of a number of specific case studies (includingthose cited in the Introduction, above), current know-ledge is, in any case, insufficient to permit the formula-tion of a general predictive model at this level.

8. Conclusions

The thesis developed in this account is that provided anadequate means of categorizing and describing theplanktonic vegetation can be formulated, it is possibleto relate phytoplankton periodicity to broad seasonalchanges in the physico-chemical environment. Here the

156 HOLARCTIC ECOtOOY 3:3 (1980)

composition of the phytoplankion has been brokendown into 14 discrete assetnblages, whose temporalsequences follow one of three directions: autogenic suc-cession (determined principally by nutrient availabilityin a relatively steady physical environment), reversion(brought about by brief physical perturbations of theenvironmental structure, followed by a return to condi-tions similar to those obtaining in the previous 'steadystate') and shift (following a more prolonged physicalperturbation, equivalent to the estabhshment of a 'new'steady state).

The principal autogenic sequence follows the onset ofstable thermal stratification in spring: in the more eut-rophic systems, vernal diatom populations are replacedby assemblages dominated first by Volvocales [3] thenNostocales [6] and, ultimately, by the Microcystis [9] orCeratium [10] groupings; the parallel succession in the'mesotrophic' systems is through theChrysophyte-Sphaerocystis assemblages [4, 5] to one inwhich Ceraiium is a prominent member. Increasedwind-mixing and epilimnetic enlargement favour theestablishment of a diatom-desmid assemblage (domi-nated by Meiosira granulata / Fragilaria crotonensis [8]in the richer lakes or by Tabellarla flocculosa, Fragilariaand Staurastrum spp. in the less rich examples). If per-sistent these changes are consistent with shift. Alterna-tively, the return to more stable conditions have, inmany instances, been followed by the re-establishmentof stages from the earlier succession (e.g. Eudorina/Volvox in Crose Mere, 1973, 1974; Dinobryon inGrasmere, 1978; Ankyra In Enclosure A, also during1978). These examples are arguably cases of reversion.

The many factors which together influence the out-come of within-assemblage selection of the dominantspecies have not been considered here. Some of thesesame factors may themselves be responsible for ad-vancing the assemblage succession independently. It hasbeen shown that frequent nutrient enrichment of theLund Tubes did not remove the alternation between themaxima and minima of biomass, but that these fluctua-tions may have been related to the growth strategies ofthe algae themselves. This observation in particularconditions the still widely-accepted view that seasonalperiodicity is explicable largely in terms of nutrient av-ailability.

Another possible mechanism is grazing. Severalpopulations which were eventually removed largely byfilter-feed ing zooplankton (unpubl. data) may have ap-peared earlier or later or not at all, or persisted longer,had the animal population been different. In this sense,periodicity was under biotic rather than physico-chem-ical control. On the other hand, to have constituted themajor element of a dominant assemblage at all the de-veloping populations tolerated some grazing pressure.The plankton communities investigated were alwaysresultant upon the sum of all the processes regulatingphytoplankton populations acting in concert. By impli-cation, the observed assemblages have been subject to

grazing. In other words, communities described shouldbe regarded not as the menu, but as the unserved por-tion of the meal.

The major conclusion I wish to draw from this study isnot that seasonal periodicity can be exclusively resolvedin terms of the physical structure of the environment, orof the availability of nutrients within it, but that thesetwo factors are, directly or indirectly, the most impor-tant variables likely to influence the general composi-tion of the phytoplankton. This hypothesis should betested experimentally.

Acknowledgements — Although the analyses, interpretationsand opinions presented in Ihis account are my own, it isnevertheless a pleasure lo record my gratitude to a largenumber of colleagues who have assisted in the collection andprovision of the basic factual data. Messrs K. Shepherd and F.Prickett collected the samples from Windermere, and also pro-vided the temperature data; Mr. J. D. Allonby collected mostof the samples from Grasmere, while the samples and fielddata for Rostherne Mere were obtained and dispatched by Mr.J. Osborne and latterly by Mr. D. A. Rogers, with the co-oper-ation of the (then) Naiure Conservancy. The data for theBlelham Tubes were obtained with the capable assistance ofMr. M. J. Nield and Mr. B. M. Godfrey, supported at differenttimes by Messrs J, Bushrod, C. Walton and D. Dand, Dr. A. J.D. Ferguson, Dr. A. E. Irish, Miss Pauline Young and MissSheila Wiseman. I am also grateful to Dr. J. G. Jones whoprovided the temperature data for Grasmere, to Mr. G. H.Hall for hydraulic retention data for Ihe same lake, to Dr. J, F.Tailing, F. R. S. who allowed me to use his chlorophyll deter-minalions for Windermere, and to Dr. J. W. G. Lund. C. B. E.,F. R. S. and Dr A. E, Irish for permission to include dataconcerning Blelham Enclosure B for 1976. The chemicalanalyses for Windermere, Grasmere and the Blelham Enclos-ures were performed by Messrs J. Heron, E. Rigg and C.Woof. I am especially indebted lo Dr. J. W. G. Lund, Dr. J. F.Tailing, Dr. D. G. George and Dr. A. E. Irish who providedhelpful criticisms of successive drafts of the final manuscript.The Department of the Environment, who provided partialfinancial support for the work on the Blelham Tubes(DGR/480/310) and the Trustees of the Cole Mere, are alsogratefully acknowledged.

A shortened version of this paper was read at the FreshwaterBiological Association's Golden Jubilee Symposium, held atthe University of Lancaster, U.K., 17-19 July, 1979.

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