Hydrobiologia 424: 147–152, 2000.C.S. Reynolds, M. Dokulil & J. Padis´ak (eds), The Trophic Spectrum Revisited.© 2000Kluwer Academic Publishers. Printed in the Netherlands.

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Understanding the assembly of phytoplankton in relationto the trophic spectrum: where are we now?

Colin Reynolds1, Martin Dokulil2 & Judit Padisak3

1Freshwater Biological Association and Institute of Freshwater Biology,The Ferry House, GB-LA22 0LP Ambleside, U.K.2ÖAW Institut für Limnologie, A-5310 Mondsee, Austria3University of Veszpr´em, Institute of Biology, H-8201 Veszpr´em, Hungary

Key words:phytoplankton, lake typology; trophic status; community assembly

Abstract

An overview of the eleventh IAP Workshop is presented. Although significant progress has been made in therecognition of the factors governing species selection at differing trophic levels, it is recognised that the ultimateinfluences of species composition are precedent and stochasticity. No individual species is selected uniquely bya given combination of environmental conditions, although there are functional and morphological traits whichpre-adapt some species above others to function preferentially in either oligotrophic or eutrophic conditions. Withthis in mind, a new set of rules of community assembly is offered.

Overview

This concluding editorial summarises some of theplenary discussions at the eleventh Workshop of theInternational Association of Phytoplankton Taxonomyand Ecology (IAP), held in August 1998, at PrestonMontford Field Centre, near Shrewsbury, UK. Theprincipal intention is to record the benchmark of aconsensus of understanding reached by the Workshopparticipants and to draw from the presentations anddiscussions a perception of the progress that the IAPWorkshops have achieved.

To do this, we must once again emphasise thestarting conditions. The Granada Workshop had beensignificant in conception and explicit in its acceptancethat there are real qualitative differences in phyto-plankton composition between oligotrophic and eu-trophic lakes. It is no less significant that the diffi-culties that were encountered have seemed so funda-mental. Rojo et al. (2000, this volume) have summar-ised eloquently the dilemma: although there are com-mon, sound intuitions about what constitutes eutrophicor oligotrophic plankton, established in numerous ob-servations and experiments, few patterns of assemblyhave been recognised or associated with the relevantdimensions of trophic state. Much less is there any real

basis for predicting structures. Moreover, as Naselli-Flores (2000, this volume) reminds us, similar phyto-plankton assemblages may be encountered in lakes ofsupposedly quite different trophic states (based, forexample, on OECD categories) and, conversely, lakesjudged to be trophically similar may differ in the spe-cies structures they support. Sometimes, difficultiesarise because of the proximity to a nutritional shift,as a consequence of a recent eutrophication or restor-ation. In such instances, existing species assemblagesmay persist for some time. This ecological inertia canconfound any judgement about the conditions that thespecies are supposed to characterise: trophic switchesand compositional responses may become confused(Dokulil, manuscript in review). It is humbling to con-cede that, despite an enormous investigative effort tounderstand the factors regulating species compositionin the phytoplankton, the forces governing selection,dynamics, diversity and stability ‘remain mysteries’(Tilman, 1996).

Only the quantitative responses of the phytoplank-ton biomass seem to be anywhere close to beingpredictable on the basis of the nutrient supplied. Thismuch is, of course, very well known already. Whenit comes to species composition, no such convenientsurrogate is demonstrable. Basically, the mechanisms

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of species selection remain controversial, the rules ofcommunity assembly are poorly understood and thecomposition of assemblages is too stochastic to bepredictable, except, perhaps, at some higher level ofclassification.

The 1998 workshop tried to focus on these broaderpatterns and on their explanative mechanisms. Thespecific question relating the trophic state of a waterbody to the pattern of species it is likely to supportwas addressed directly in several of the presentations(Beyruth, 2000; Borics et al., 2000; Huszar et al.,2000; Leitão & Leglize, 2000; Temponeras et al.,2000; all this volume). Intuitive assumptions are madeby experienced heads. This intuition is revealed as wemove among authors and among lakes, each confid-ent about the kinds of environment in which speciesA, B or C normally live but from which D and Eare generally well-understood to be excluded. Thewidespread use of tools such as CANOCO (canonicalcorrespondence analysis: Ter Braak, 1987) helps toconfirm and formalise the suspected grouping of thespecies encountered.

However, we still seem too poorly equipped todetermine the decisive traits of the species which,apparently, cluster on ecological lines. Is it, per-haps, some preferred range of nutrient availability or,possibly, some particular source of phosphorus or ni-trogen? Or is it something to do with the ratios inwhich nutrients are supplied that influences the se-lection of species (see, for instance, Teubner et al.,1999)? Even supposing the latter to be the case (acounterview was put at the Granada workshop), noreally predetermined pattern of compliance has beenidentified, except at chronically low concentrations ofkey nutrients, where critical limitation of phytoplank-ton growth rates is demonstrable, and where specieswith a proven high-affinity uptake capability are ableto gain advantage.

Such uncertainties are multiplied when we are con-fronted by a list of physical and chemical attributesof a particular lake and an invitation to nominatedominant algae. This was precisely the challenge ofthe ‘Design-a-plankton’ exercise (Reynolds 2000, thisvolume), where the confidence of intuition and ex-perience was quickly usurped by self-doubt and areluctance to speculate. Again, the trepidation is an-ticipated in Rojo et al. (2000, this volume), who saythat ‘We do not know that an association [of algae] in-habits a specific environment . . .’; rather, recognisablepattern is achieved because certain algae may implya particular trophic state, not because there is any ele-

ment of any “ . . . prescription that ‘in this trophic state,we will find this alga’ ”.

Nevertheless, the recognition of pattern amongthe higher levels of species structure among theassemblages from different categories of lake waspalpably stronger at the 1998 Workshop. It is ofgreat interest to find that several contributors (Beyr-uth, 2000; Borics et al., 2000; Huszar et al.,2000; all this volume) were prepared to go bey-ond the mathematically-sorted groupings by seekingto relate the preferred growth conditions of definedspecies-clusters to particular limnological conditions.The application of association labels to frequentlyco-occurring species of phytoplankton or alternativedominants, inspired by the approaches of the lead-ing phytosociologists (Braun-Blanquet, 1964; Tüxen,1955), is relatively new and is still at a primitivestage of development. The success achieved by theseauthors in fitting their observations to a pre-existingscheme of classification is surely a vindication of thisapproach to description of high-level pattern. The de-velopment of this approach and the refinement of thecategories can be recommended with confidence.

To be able to move from pattern recognition to ex-planation of process and prediction of outcome is stillsome way off. There are, however, some helpful point-ers of the direction that should be taken. For instance,reproducible, non-random, co-occurrences of differ-ent species of phytoplankton are strongly suggestiveof a commonality of responses to a given combin-ation of environmental conditions. Just as clearly,this behaviour is often attributable to some adaptivetrait(s) that the co-occurring species share in common.To take a straightforward example, the frequently-observed simultaneity of occurrence of populationsof Anabaenaand Aphanizomenonspecies in strati-fied, mesotrophic lakes, especially when there is adeficiency in the nitrogen supply, is related to theircommon abilities to maintain themselves in the surfacemixed layer (regulation of the buoyancy imparted byintracellular gas vesicles), to enhance carbon uptakeat high pH (carbon-dioxide concentrating transport)and to free themselves from dependence on a supplyof combined nitrogen (dinitrogen fixation in special-ised heterocytes). More subtle traits must distinguishamong the preferred environments of (say) large di-atoms and large dinoflagellates, or ofCosmarium,PandorinaandGemellicystis. The fact that these al-gae are often distinguishable on morphological criteria(volume, surface area, carbon-specific projection, etc.:Reynolds, 1997) provides only part of the functional

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explanation. Nevertheless, to be able to match theselective criteria proposed for each identified speciescluster (‘Association’, in Appendix II of Reynolds,2000, this volume) to the known environmental con-straints in a given body of water offers a coarse levelof prediction of the species associations likely to berepresented, on the basis of their traits.

Perceptions

In the discussion sessions, the Workshop sought somegeneral perceptions of the patterns implicit in theconcept of a trophic spectrum and the extent to whichit might ever serve as a predictive tool for man-agement. There was general agreement about theaspects of phytoplankton community ecology thatwere stochastically driven and ultimately unpredict-able. Species-specific dominance, maximal populationsize, date of its achievement were all important factsin the reporting of events in the plankton ecology of agiven system which all depended upon a complex ofinputs, involving system memory of past events andforwarded inocula (Padisák, 1992), weather eventsand their influence on the physical limnology of thewater body (Dokulil, 1999), as well as parallel impactson the loads of nutrients delivered in any one grow-ing season, both from its catchment and from withinthe body itself. Moreover, these effects could be fur-ther confounded by internal biotic variations, affectingthe nature and intensity of zooplankton grazing andof fungal parasitism. Recruitment from the sediment(overwintering populations, resting stages, etc.) mayalso be of relevance (e.g., Head et al., 1999).

Doubts persist about the extent to which interactiveprocesses (especially interspecific competition, preda-tion, parasitism) determine community structure andwhether, however well they may be quantified, theycan account consistently for the species representationand richness of assemblages at any given location.

The perception of the workshop participants wasthat community assembly is a complex process andsubject to a great deal stochasticity. We could just aseasily and, perhaps more usefully, view the problemfrom the standpoint of a null hypothesis that there is noover-arching regulation of phytoplankton distribution(Rojo et al., 2000, this volume). Let us say that “allspecies are everywhere and will produce populationswherever and whenever they can”. A great numberof observations and a welter of experimental evidencesuggests that this hypothesis does not always hold, so

it appears not to be continuously inviolate. Therefore,we need to have an idea about the frequency and theextent of the violations. For instance, we know thataggregations of species occur (assemblages) and weknow that certain combinations of species are morelikely than others (associations), because the extentof their departure from stochasticity is statisticallymeasurable.

Now, we should ask the question, how and to whatextent does the position of a lake on a trophic spectruminfluence the aggregation of species in a way whichleads us to recognise the representation of distinctiveassociations? We can see at once that this approach de-tects that resolution of the issue is impossible withouta clear understanding of precisely what environmentalvariability is described by the trophic spectrum.

What is the Trophic Spectrum?

In much the same way as the OECD schemes hadfoundered, two decades previously, in nominating theprecise nutrient concentrations dividing eutrophic sys-tems from mesotrophic ones, and mesotrophic fromoligotrophic ones, it was considered premature andprobably impossible to nominate the nutrient concen-trations to delimit the occurrences of intuitively dis-tinguished ‘oligotrophic’ or ‘eutrophic’ assemblagesof phytoplankton. Moreover, some of these differ-ent assemblages live within similar ranges of nutrientconcentration. The answer to this conundrum is thatthe concept of trophic state invokes important com-ponents of lake metabolism other than nutrient avail-ability, including physical mixing, light availability,carbon dynamics and a whole host of biotic influ-ences. Even the availability of nutrients is complicatedby the variety of phosphorus forms (inorganic or or-ganic, bioavailable or irretrievably bound to minerals)and available nitrogen species (nitrate, ammonium,dinitrogen) likely to be present. This complexity hadbeen recognised in Granada, when it was concludedthat there is no single axis of variability and there isno single relationship that will ever predict the floristiccomposition of the phytoplankton of a lake from thequantities of nutrient it receives.

In order to be able to offer even a qualitative ex-planation for consistent patterns of distributions ofplanktonic associations in relation to lake trophy orto be able to make probabilistic predictions of theirrepresentation when trophic state is altered, we stillrequire to have a sharp appreciation of the relevant

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environmental variability that the conceptual trophicspectrum implies and of the biotic sensitivities onwhich it impinges.

Reaching consensus on this last point involved aninteresting, brainstorming exercise in lateral thinking.Among the more memorable suggested definitions forthe Tropic Spectrum were:

‘A continuum of algal assemblages through a com-bination of environmental gradients’

‘Variation in assemblage structure, biomass andabundance’

‘The range between two different levels of nutrientenrichment’

‘Algal assemblages express levels of primary pro-duction in reflection of limitingresources’

One moved to higher ecological theory with ‘Gradientof accumulation of potential energy as organic mat-ter [exergy] and of decrease of dissipation through thefood web. Yet closer to Ulanowicz’ (1986) theories,was the thought-provoking ‘Continuum of total systemthroughput in an excess of information flow’.

It may be noted that any reference to nitrogenor phosphorus or the ratio between their concentra-tions was conspicuously absent from this exercise.The reluctance to even name phosphorus as a factorin plankton selection demonstrates a remarkable shiftin the collective mindset towards a commitment toa more holistic view of plankton systems and theirmetabolism. This point was conceded in the interimdefinition that was agreed:

The Trophic Spectrum is a conceptual recognitionthat fresh waters of differing metabolic potential sup-port organisms consistent with the level of productivitysustainable within the capacity of the relatively leastavailable of the constraining resources.

Although phosphorus enrichment is correctly re-cognised to have been a major factor in lake eutroph-ication, it may also lead to a switch in the criticalmetabolic constraint to other factors or factor inter-actions. In turn, these too impose selective biases infavour of species whose growth and survival are rel-atively more tolerant of conditions of chronically lownitrogen, carbon or light. The provisional definitionretains the utility of the pattern recognition but doesnot prescribe more than the algal attributes likely to beof selective advantage.

Rules of community assembly

This then provides a bridge to the proposal that spe-cies sharing common selective advantages make themrelatively stronger contenders to be well-placed in theassemblage that may develop, along with other spe-cies, able to fulfil the same selective criteria. Weaccept that certain algal attributes or traits are nowmore likely to be favoured than others, therefore somespecies will always be more likely to occur than oth-ers. ‘Association’ labels should anticipate the speciesclusters, much as they might drop from CANOCO or-dinations (ter Braak, 1987). None of those so favoured,however, is guaranteed to be present in sufficient num-bers, or even at all, to feature prominently in the groupof supposedly ecologically similar species selected inthe lake. The group(s) thus favoured should be pre-dictable but the precise composition of the communityand the manner of its assembly are not. Assembly issubject to opportunities provided stochastically andexploitation of which is, normally, supposed to bestrongly influenced by precedent and the extent of sys-tem memory embodied in the starting inocula. In spiteof this, instances of abrupt change can sometimes bemarked by abundances of species previously scarce atthat location, as exemplified by the recent ‘sudden’appearance ofCylindrospermopsis raciborskiiin theAlte Donau (Dokulil & Mayer, 1996).

The following ‘rules of assembly’ were debatedand agreed by the Workshop participants:

(1) provided suitable inocula are available, plank-tonic algae will grow wherever and wheneverthey can and to their best potential under theconditions obtaining;

(2) then, of those present, the species which are ini-tially likely to become dominant are those able tosustain the fastest net growth rates and/or thosearising from large inocula;

(3) the species with the largest autochthonous in-ocula are generally those which have been abund-ant at the same location in the recent past.

(4) environments may select preferentially for cer-tain algal attributes or traits;

(5) species with preferred attributes are likely tobuild bigger populations and, where appropriate,to found larger inocula to carry forward;

(6) phytoplankton assemblages become biased intheir species composition with respect to theconditions obtaining in individual water bodies;

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(7) the species most frequently characterising spe-cific environmnents share common advantageousattributes;

(8) the outcome of community assembly is subject tofood-web and other interactions;

(9) of those species present (and quite independentlyof the initial conditions), the ultimate dominant islikely to be the one with the most advantageousadaptations;

(10) assembly is always subject to the overriding ef-fects of environmental variability and of the re-setting of assembly processes.

Two points made during the discussion leading to theformulation of these rules may be noted. One wasthat the Trophic Spectrum provides a matrix in whichthese rules might operate. The other, the use of hab-itat templates, as conceived by Southwood (1977)and parameterised to distinguish the critical dimen-sions of aquatic habitats (Reynolds, 1987, a.o.), of-fers a promising tool for investigating and evaluatingcluster-selective mechanisms.

Conclusions

This commentary on the deliberations of the eleventhIAP Workshop records several areas in which intellec-tual progress has been achieved, to the extent that an-swers to the question in the title, ‘Where are we now?’,may reasonably be ventured. First, there is a broadacceptance that lakes of different trophic state sup-port mutually distinct assemblages of phytoplankton,though the patterns determined rely upon the presenceof certain algae indicating a given trophic state ratherthan the trophic state determining which algae mightbe there. It has also been established firmly that spe-cies clusters or associations are more helpful and moreconsistent in detection of pattern than are the presenceof individual ‘indicative’ species. The idea of usingmathematical sorting methods to identify clusteringin real data and the persistent trends in the matchingof morphological and physiological traits to ecologiesoffer the real prospect that the probabilistic predictionof representation by recognised species-associations isan achievable goal.

That the mechanisms of selection, for or against,the traits common to the species of particular as-sociations or clusters are not confined to the singledimension of phosphorus availability is also strongly

established. Much more important is the recognitionof a series of critical factor interactions, arising fromthe metabolism of the whole system (albeit alterableby phosphorus, or any other potentially limiting inputvariable). The spectrum turns out not to be a singleaxis but a multi-dimensional matrix, which may beanalogised to habitat template models. The Workshopalso explicitly recognised that phytoplankton compos-ition does not vary as a series of bands on (say) aVollenweider-type regression. Species selection, evenwithin the broader view of the Trophic Spectrum ad-opted here, remains strongly subject to stochasticityand precedent: qualitative responses to trophic enrich-ment can be predicted only as probabilities but, asmore becomes known about the physiological capab-ilities and limits of the individual species of algae,so the mathematical acuity of the probability may beimproved.

Acknowledgements

This article is predominantly based upon the finalplenary discussion of the Workshop. The authors aregrateful to all the participants for their willingnessto contribute freely of their knowledge and ideas.Special thanks are due to Dr Ingrid Chorus, whochaired and guided the discussion with sensitivity andconsummate skill.

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