have been some experiments with these (Kentucky Division of Biology 1994; Hill et al. 2000) but more work is .... Technical Report No. 51. Frankfort, Kentucky.
Nova Hedwigia, Beiheft 130, p. 357-372
June 2006
From pattern to process: understanding stream phytobenthic assemblages and implications for determining "ecological status" by
Marian L. Yallop1' & Martyn G. Kelly2 1
2
School of Biological Sciences, University of Bristol, Bristol , BSa 1UG '- UK Bowburn Cons ultancy, 11 Monteigne Drive, Bowburn, Durham DH6 50B, UK
With 5 figures and 1 table
Yallop , M.L. & M .G. Kelly (2005): From pattern to process: understanding stream phytobenthic assemblages and implications for detennining "ecological status" . - Beiheft zur Nova Hedwigia 130: 357372 .
Abstract: Phytobenthic communities are important primary producers in streams. We draw upon some key studies on these assemblages from Europe and elsewhere, highlighting those which have had a significant impact on our understanding of the structure of these complex communities and survey how fundamental knowledge has been used to develop practical tools for use within the water industry. We consider how these communities can be used to develop a dynamic and process-based understanding of "high" , good" and "moderate" ecological status" as required for the European Union Water Framework Directive.
Introduction Over the past 25 years several indices based on algae have been used routinely by water management bodies throughout Europe and beyond (Prygiel & Coste 1993; Kelly & Whitton 1995; Rot! et al. 1999) with much of the work stimulated by legislation such as the Urban Wastewater Treatment Directive (UWWTD: European Community 1991). Matters have progressed significantly since Round (1981) , in his seminal work Ecology of Algae, commented that "the study of algae in rivers has hardly begun". Yet , as we read this statement a quarter of a century later, we feel a profound sense of irony. Whilst this applied research has increased our knowledge of how benthic algae (and diatoms in particular) respond to chemical variables associated with pollution gradients, the approach has often been to treat benthic algal assemblages as practical "tools" from which the state of the environment could be inferred. In this
.. Corresponding author
1438-9134/01/0130-357 $ 4.00 © 2006 J . Cramer in der Gebr. Borntraeger Verlagsbuchhandlung , D·70176 Stuttgart
358
Marian L. Yallop & Martyn G. Kelly
paper, we argue that the focus on pollution gradients that led, particularly in Europe, to the development of practically-orientated indices, has been at the expense of a genuine understanding of how stream algal communities function. Research has moved from describing stream algal communities in relation to environmental gradients to deriving practical indices without necessarily understanding community-level processes. Whilst the study of how taxa are distributed along environmental gradients improves our understanding of the autecology of those taxa we argue that synecology is more than the sum of the separate autecologies. Round's (1981) observations are particularly relevant to the most recent European legislation that adopts a new approach to water management. Whereas earlier legislation defined environmental quality in terms of the absence of undesirable properties (typically chemical pollutants), the Water Framework Directive (WFD: European Union 2000) defines it in terms of positive attributes such as "good ecological status" (GES) or, in layman's terms, the presence of a healthy, natural (or near-natural) biota with only "Iow levels of distortion" resulting from anthropogenic activity. " Phytobenthos" is one of the biological elements that the Directive specifies as contributing to "good ecological status" and this , in turn , poses intriguing questions for phycologists. In particular, if the focus is on the (near-) natural biota, then we need to know about the structure and function of such communities , their variability in space and time and be able to assess deviations both above and below GES in order to establish boundaries. Furthermore , we need be able to assess what implications such natural variation will have on implementing practical monitoring regimes. The development of methods appropriate for legislation such as the WFD will, in other words, require a paradigm-shift away from a narrow fixation on environmental gradients and towards monitoring techniques that adopt a more hol istic approach . Studying stream algal communities is not easy. Apart from the spatial and temporal heterogeneity within any reach, the small size of many organisms makes studies of the structure of communities in situ very difficult. Either artificial substrata are adopted (which have their own problems: Cattaneo & Amireault 1992) or destructive sampling methods are required. Sampling a community and preparing a wet mount for analysis under the microscope will disrupt interrelationships amongst the constituent taxa and their substrata. The prevailing dogma of recent years has been that names and relative abundances of even rare constituents of the community provide valuable data for monitoring . Moreover, the use of indices requires that data are summarised in the form of relatively simple metrics which, again, means that higher order information about the community is lost. The ability to produce a usable metric from one constituent of the phytobenthos (typically diatoms) has great practical advantages , particularly as it limits the number of taxa that any analyst needs to know. Diatoms are particularly amenable to study as the siliceous frustule is robust, relative to the cell structure of many other algae. Such practical benefits might be lost if a new generation of monitoring tools was based on all the constituents ofthe phytobenthos . On the other hand , is it possible , we wonder, to translate our understanding of the processes governing the entire stream biofilm community into a method that preserves the practical advantages of diatom-based indices? These questions are too big to expect definitive answers in a short review. Our approach is to consider to what extent our understanding of these complex communities has developed over the last few decades. In the process of comparing "what they knew then " with "what we know now" we will address issues that are relevant for the practical assessment of "good ecological status" using diatoms, in particular. We will develop a theoretical framework upon which a new generation of methods can be developed . Our primary focus is the UK, but many of the observat ions will be relevant further afield.
From pattern to process
359
Historical perspective The first detailed quantitative study of river-bed algae was that of Geitler (1927) working on an Austrian mountain stream. Apart from the descriptive account of Fritsch (1929) , working on stones in streams in Devon, the first quantitative data from the UK are those of Butcher (1932 , 1940, 1946, 1947) and Butcher et al. (1937), working under the auspice's of the Water Pollution Research Board . He used glass slides to enumerate sessile algae from several rivers including the Lark, Itchen , Tees, Tern, Cam, Skeme and Hampshire Avon and concluded that diatoms were both the most abundant and most diverse group of algae although two other groups , the Chlorophyta (particularly the Chaetophorales) and Cyanobacteria (particularly the Chamaesiphonales) were also important (Butcher 1932). Butcher linked the communities that he observed to particular environmental conditions. A correlation between algal growth and degree of organic pollution was demonstrated in the River Trent, and further supported with data from the Tame, Bristol Avon and Chumet (Butcher 1947). In "polysapropic conditions" (tenninology of Kolkwitz & Marsson 1908) where the rate of organic decay is relatively high, the dominant species was Stigeoclonium tenue with Nitzschia palea (Kiitfing) W. Smith and Gomphonema parvulum as subdominants. He noted that the latter two diatom species become dominant further downstream in "mesosaprobic" conditions and then decreased , to uncommon in "oligosaprobic" conditions where Cocconeis placentula, Chamaesiphon spp. [including C. incrustans Grunow and C. britannicus (F.E. Fritsch) Komarek & AnagnostidisJ and Protoderma frequens (Butcher) Printz dominated. Observations were also made on changes in the benthic algal communities in relation to nutrient gradients on the River Tees . Communities in the upper "oligotrophic" reaches were dominated by the "Achnanthes spp." complex (now Achnanthidium, Rossithidium and Planothidium spp.) and were replaced by communities dominated by Cocconeis placentula further downstream where the river was more "eutrophic" (Butcher et al. 1937). Butcher (1946) also examined temporal patterns, grouping rivers into two major types , one showing no clear seasonal periodicity, with a "climax community" of diatoms including Gomphonema olivaceum (Hornemann) BnSbisson, Achnanthidium minutissimum, Nitzschia palea, Gomphonema parvulum and "Achnanthes lanceolata (Bn:bisson) Grunow" (Plan othidium spp.), present all year around. Other rivers had a distinct spring diatom community with species that were rare in the first group of rivers [e.g. "Navicula viridula (Kiitzing) Ehrenberg", Surirella ovalis Brebisson and Ulothrix zonata J. Observations such as these have particular practical relevance for determination of present-day sampling regimes. After the pioneering work of Butcher, river algae in the UK were neglected, relative to other groups of organisms (e.g. invertebrates) and other freshwater habitats (e.g. lake plankton) until the 1960s when studies of stream algal communities had started to diverge in two directions. The predominant approach in mainland Europe was to consider stream algal communities with respect to environmental gradients, particularly those linked with environmental pollution. This led to development of indices for pollution monitoring. Early work included that of Zelinka & Marvan (1961) and Si300 m above sea level) where human population density is relatively low and there are fewer obvious human impacts (although, in some remote areas of Scotland and Wales, such streams may be found closer to sea level). . The harsh climate .o f these areas makes scouring spates relatively common and it is easy to envisage a cobble or small boulder that has been scoured and rolled by a storm such that it presents a bare (or almost bare) surface for colonization. Biggs et al. (1998) describe five traits that facilitate the success of such taxa: they are small, have high resistance to removal by hydrological disturbance, high immigration rates, high growth/vegetative reproductive rates and low half saturation coefficients for nutrient uptake. Achnanthidium minutissimum (syn. Achnanthes minutissima) fulfils all these conditions and is the most common species found in circumneutral upland streams (Fig. 3). There is considerable taxonomic confusion around Achnanthidium and its close relatives , and it is likely that the A. minutissimum that is commonly described is actually a species complex that is difficult to differentiate with the light microscope. Even those forms that are relatively easy to distinguish [Achnanthidium biasoleitianum (Grunow) Bukhtiyarova, A. microcephalum Kiitzing fo. scotic(l J .R . Carter] are almost always found in mixtures withA. minutissimum. However,A. minutissimum is not the only colonizer that is found . Occasionally, Achnanthes oblongella Oestrup is found in abundance or in mixtures with A . minutissimum although the factors governing its abundance are not clear. In more acid habitats, Eunotia spp. fulfil the role of primary colonizers and Gomphonema parvulum is also found sometimes, across a wide range of nutrient concentrations. As the biofilm increases in thickness, competition for resources will become more intensive (Fig. 4). The biofilm contains both autotrophic and heterotrophic components that secrete polysaccharides for various reasons (stalks and locomotion in diatoms , protective slimes for other organisms) and these form a matrix, protected from the scouring action of the current, into which other organisms can colonise. Long-stalked diatoms such as Gomphonema acuminatum Ehrenberg are able to grow above the short-stalked species and avoid shading whilst more loosely-attached species such as Hannaea arcus (Ehrenberg) R.M. Patrick, Meridion circulare, Tabellariafiocculosa (Roth) Kiitzing and filamentous forms such as Fragi/aria capucina Desmazieres become entangled and are able to establish in the polysaccharide matrix
Fig. 3. Diagrammatic representation of a diatom-dominated epilithic biofilm in the pioneer stage of the trajectory illustrated in Fig. 2. Early colonists such as Achnanthidium minutissimum (a) and Cocconeis placentula (b) occupy space on the upper surface of the rock, along with bacteria (c). Scale bar: IO /tm.
366
Marian L. Yallop & Martyn G. Kelly
Fig. 4. Diagrammatic representation of a diatom-dontinated epilithic biofilm at an intermediate point in the successional trajectory illustrated in Fig. 2. Cell division by pioneers along with further immigration leads to competition for space within the biofilm. Short-stalked erect species of Gomphonema (d) and Meridion circulare (e) have a competitive advantage as the biofilm increases in thickness. The quantity of polysaccharide matrix (f) increases. Scale bar: ID /lm .
(Fig. 5). Non-diatom algae are also found in early-stage biofilms, although they are usually less abundant. These include filamentous green algae such as Ulothrix, non-heterocystous Cyanobacteria such as Phormidium along with representatives of several other algal divisions. Clearly, a range of processes is operating to generate the diversity that is observed within and between streams. These processes fall into two broad types: those that influence the entire reach (e.g. nutrient availability, pH, hydrology) and those that work at a finer scale (e.g. related to the size of substratum). The latter, in particular, can mean that several trajectories from the pioneer state are possible at anyone site, depending upon the microhabitat. It is common to find cobbles and small boulders in upland streams that have biofilms dominated by diatoms . Nonetheless, the end-points of Biggs et al.'s (1998) successions are largely ", non-diatom algae (16 out of 22 taxa) . The most likely reason for the abundance of diatoms in upland streams may simply be that frequent scouring spates and/or intensive grazing prevent the successions proceeding beyond the point where these other taxa are able to establish on all but the largest boulders and bedrock. Indeed, the mix of substratum sizes - and corresponding vulnerability to disturbance - creates a heterogeneous stream reach which, in turn , means that several stages of the "trajectory" can co-exist, leading to a "patchy" and therefore diverse flora. Another characteristic of the taxa that Biggs et al . (1998) regard as end-points of the succession is that they tend to have a filamentous or colonial, rather than unicellular, growth form . The exceptions (e.g . Rhoicosphenia) are taxa that are typically epiphytes. The S-strategists listed in Table 1 include both nitrogen fixers (Nostoc. Calothrix, Epithemia, Rhopalodia) and taxa known to be able to use organic phosphorus sources (Draparnaldia. Calothrix). Interestingly, the taxa that Biggs et al. (1998) regard as "C"-strategists are most conspicuous in enriched streams rather than "natural" conditions. particularly in upland environments. Under such conditions, "S"- and "C-S"-strategists are usually more conspicuous although Cstrategists such as Cladophora are found, albeit in smaller quantities than in enriched streams.
From pattern to process
367
Fig. 5. Diagrammatic representation of a diatom-dominated epilithic biofilm at an advanced stage of the successional trajectory illustrated in Fig. 2. Intensive competition for space favours large erect taxa such as Synedra ulna (g) and Gomphonema acuminatum (h), and filamentous taxa such as Tabellaria jlocculosa (i) grow entangled in the biofilm . Motile taxa such as (j) are able to move through the biofilm and sediment particles (k) become trapped in the biofilm whilst the algal biomass attracts grazers such as Paramecium (I). Scale bar: 10 I'm .
If the physical heterogeneity of the habitat provides a primary structure to the benthic flora present at a reach, then the co-existence of several different macroalgal taxa can add to the diversity of habitats available for diatoms and other microalgae to colonise. The new habitats available will include attached algae growing epiphytically as well as algae in looser associations (e .g. Ulothrix spp., Fragilaria capucina, Tabellariajlocculosa) whilst motile diatoms will be able to move in and around the filaments and the finer sediments that these invariably trap. Achnanthidium minutissimum is a common epiphyte at low nutrient concentrations, highlighting the essentially opportunistic nature of this and many other diatom species . Large substrata that are moved by only the strongest floods present an interesting test of the ideas of Biggs' et al. (1998) . Where a mature biofilm is able to develop, we suggest that the trajectory will extend to Chantransia stages of red algae such as Lemanea that can overwinter and develop into mature thalli the following spring or, alternatively, moss protonema that can colonise and develop into gametophytes . However, in many cases , the theoretical "end-point" will not be reached, as the substrata will be turned over during larger spates or the biofilms will be scoured away. This will prevent the biofilm growing beyond the diatom-dominated stages although it is possible that slow-growing encrusting (or, in a few cases, endolithic) algae will be able to establish partly due to a flat , ultrastreamlined growth form. Examples of
368
Marian L. Yallop & Martyn G. Kelly
such taxa include the red alga Hildenbrandia , the chlorophyt, Gongrosira incrustans (Reinsch) Schmidle, the cyanobacteria Phormidium incrustatum Gomont ex Gomont and Chamaesiphon spp. as well as lichens such as Verrucaria. Such communities are similar to those found growing on the granite flatrock in the piedmont of the southeastern United States (Everitt & Burkholder 1991). None of these taxa fit neatly into the two-dimensional conceptual model and represent, perhaps, a group tolerant to a stress that occurs on a different axis to those envisaged by Biggs et al. (1998) .
Conclusion: Implications for monitoring ecological status The purpose of this review is not to disparage existing diatom-based indices, several of which are playing a valuable role in the management of water quality in Europe. Instead, we wish to point out the limitations of such methods from the point of view of new legislation such as the WFD. Existing approaches are "fit-for-purpose" in that they provide objective information on the response of the biota to particular environmental pressures that can inform decisions about future investment in water treatment facilities . However, the WFD requires a paradigm shift in our approach to monitoring in Europe, insofar as ecology is now the ultimate, rather than the proximate, goal of water management. Whilst it is possible to define GES in terms of threshold values of existing indices, the essentially univariate nature of the assumed to gradients underlic these indices assume means that unexpected pressures may be missed. There is an underlying circularity of reasoning: assumptions about the nature of pressures dictate the choice of metrics that, ultimately, influences which pressures are detected. A more appropriate approach would be to define the reference state of the phytobenthos and then to measure deviations from this in a manner that makes no assumptions about the nature of the pressure . This is essentially the essence of the Directive. However, the dynamic nature of stream ecosystems means that some taxa, "expected" under reference conditions, may be missing simply because the wrong point on the trajectory was sampled. The reference state in streams is, therefore, better understood as a cluster of possibilities rather than defined in absolute terms. This implies a need for status assessments to be based on several samples per site to encompass the spatial and temporal variation. At a simple level, such a strategy will increase the probability of detecting taxa characteristic of undisturbed conditions; however, it should also be possible for this strategy to inform a more process-based interpretation of ecological status. In effect, we are suggesting that a taxon list, derived from a number of samples from similar sites at various stages in the microsuccesional trajectories could be used as a proxy variable from which functional characteristics of the phytobenthos can be inferred. In other words , under undisturbed conditions, we should expect to find taxa with a range of life histories , habits (prostrate, stalked, erect, etc .) and physiological strategies (N-fixers, heterotrophs) . The richness and evenness of the community may also be characteristic and although several studies have shown diversity to be poor as an indicator of environmental pressures (van Dam 1982), a deviation from the expected level of diversity may, nonetheless, be an indication that the community has changed from the reference state. The paradigm shift that we advocate may mean that the time is ripe for an imaginative re-evaluation of the usefulness of diversity metrics in ecological assessment. By contrast, pressures will lead, ultimately, to major changes in the way that the biofilm functions. Nutrients, for example, may favour filamentous algae which will attract characteristic epiphytes (e.g. Rhoicosphenia) whilst, at the same time , N-fixing organisms may be outcompeted. Sediment particles trapped around the bases of the filaments will create microenvironrnents favouring motile over attached taxa and, as the microbial biomass increases, so the potential for internal recycling of nutrients (favouring taxa with heterotrophic abilities)
From pattern to process
369
will increase. A step from here would be to look at changes within a functional "guild" along an environmental gradient, rather than considering all functional "guilds" simultaneously as is the case in the present generation of indices. The challenge is to build a new generation of models that encapsulate this more processbased thinking without at the same time losing the practical advantiges of the present indices. It is possible that indice~ can be developed using a single taxonomic group (e.g. diatoms) but this should not be assumed without further testing. The simplest approach would be to use a similarity measure such as chord distance. Such an approach has some applications in relation to ecological status assessment (see Bennion et al. 2004) but the amount of spatial and temporal heterogeneity expected at a single site may mean that the signal:noise ratio is too low for this to be sensitive enough. Multimetric indices are another possible approach, and there have been some experiments with these (Kentucky Division of Biology 1994; Hill et al. 2000) but more work is required before these can be recommended on a routine basis . The means by which the metrics are combined is critical in order to give a realistic balance between Type I and Type i errors; however, multimetric approaches have the advantage that the individual metrics may individually provide early warnings of the onset of particular pressures and be useful for diagnosing the reasons for deviations from reference conditions . Alternative approaches such as Bayesian Belief Networks are also worthy of consideration as a way of including much of the information encapsulated in a multimetric index but with a more elegant means of computation. This field of research has moved a long way since Butcher and his colleagues started their work on the algae of British rivers, and since Frank Round made his first investigations . Yet we owe a large debt to these pioneer researchers. In many ways, the greatest change over the half century since the start of Frank Round's career has been the passing of powerful new legislation which has provided the incentive to distil our knowledge of freshwater algae into practical indices that can help enforce this legislation and, as a result, improve the state of the aquatic environment. As we read, in preparation for this review, we found that several ideas that more recent researchers have developed were at least implied in the early papers of Frank Round and others . His generation of scholars, schooled in a more qualitative but no less objective or rigorous school of biology than their modem counterparts, would have had an intuitive understanding of the "natural" state of rivers and we should draw upon their work in the process of making the next generation of indices. We can do no better than end with the words of Isaac Newton: "If I have seen further, it is by standing on the shoulders of giants".
Acknowledgements This publication is dedicated to Professor Frank E. Round in appreciation of his contribution to phycology.
References BEHRE, K. (1956) : Die Algenbesiedlung der Seen urn Bremen und Bremerhaven. -Veroff. lnst. Meeresf. Bremerhaven 4: 221 - 383. BENNlON, H., JUGGINS, S. & ANDERSON, N. J. (1996): Predicting epilimnetic phosphorus concentrations using an improved diatom-based transfer function and its application to lake eutrophication management. - Environm. Sci. Technol. 30: 2004-2007. BENNION, H., J. FLUIN & G.L. SIMPSON (2004): Assessing eutrophication and reference conditions for Scottish freshwater lochs using subfossil diatoms. - J. App!. Eeo!. 41: 124-138.
370
Marian L. Yallop & Martyn G. Kelly
BIGGS, BJ .F, RJ. STEVENSON & R.L. LOWE (1998): A habitat matrix conceptual model for stream periphyton. - Arch. Hydrobiol. 143: 21-56. BIGGS, BJ.F & R.A. SMITH (2002): Taxonomic richness of stream benthic algae: Effects of flood disturbance and nutrients. - Limnol. Oceanogr. 47: 1175- 1186. BIRKS , HJ.B., J.M. LINE, S. JUGGINS,A.C. STEVENSON & CJ.F TER BRAAK (1990): Diatoms and pH reconstruction. - Philos. Trans . Roy. Soc. London, Ser. B 327: 263-278. BUTCHER, R.W. (1932): Studies in Ihe ecology of rivers. 11. The microflora of rivers with special reference to the algae on the river bed. - Ann. Bot. 46: 813- 861. BUTCHER, R.W. (1940): Studies in the ecology of rivers. IV. Observations on the growth and distribution of the sessile algae in the River Hull, Yorkshire. - J. Ecol. 28: 210-233. BUTCHER, R.W. (1946): Studies in the ecology of rivers. VI. The algal growth in certain highly calcareous streams. - J. Ecol. 33: 268-283. BUTCHER, R.W. (1947): Studies in the ecology of rivers. VII. The algae of organically enriched waters. - J. Eeol. 35: 186-191. BUTCHER, RW., J. LONGWELL & FT.K. PENTELOW (1937): Survey of the River Tees , Part Ill. The non-tidal reaches. - Technical Paper of Water Pollution Research , No 6. Her Majesty's Stationery Office , London . CATTANEO,A. & M.C. AMIREAULT (1992): How artificial are artificial substrata for periphyton. - J. N. Amer. Benthol. Soc. 11: 244-256. COSTE, M. (in CEMAGREF) (1982): Etude des methodes biologiques quantitatives d'appreciation de la qualite des eaux. - Rapport Division Qualite des Eaux Lyon, 218 pp. Agence Financiere de Bassin Rhone-Mediterranee-Corse, Pierre-Benite, France. DESCY, J .-P. (1979): A new approacb to water quality estimation using diatoms. -Nova Hedwigia Beih. 64: 305-323 . DICKMAN , M.D . & M.B. GOCHNAUER (1978): A scanning electron microscopic study of periphyton colonization in a small stream subjected to sodium chloride addition. - Verb . Int. Vereinigung Theor. Limnol. 20: 1738- 1743. EUROPEAN COMMUNITY (1991): Council directive of 2 1 May 1991 concerning urban waste water treatment (Directive 91 /271 /EEC). - Official Journal of the European Communities No. L 135/4052. EUROPEAN UNION (2000): Directive 2000/60IEC of the European Parliament and of the Council of 23 October 2000 establishing a framework for community action in the field of water policy. - Official Journal of the European Communities No. L 327: 1- 73 . EVERITT, D.T. & J.M . BURKHOLDER (1991): Seasonal dynamics of macrophyte communities from a stream flowing over granite flatrock in North Carolina, U.S.A . - Hydrobiologia 222: 159-172. FLOWER, RJ. & R.W. BATTARBEE (1983): Diatom evidence for recent acidification of two Scottish Lochs . - Nature 305 (5930): 130-133 . FRITSCH , FE. (1929): The encrusting algal communities of certain fast flowing streams. - New Phytol. ' .'28: 165- 196. GEITLER, L. (1927): Dber Vegetationsfarbungen in Biichen. - BioI. Gen. 3: 791 -8 14. GRIME, J .P. (1977): Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. - Amer. Naturalist Ill : 1169-1194. GRIME , J.P. (1979): Plant strategies and vegetation processes. - John Wiley and Sons , Chichester. HARGREAVES, JW. , EJ .H . LLOYO & B.AWHITTON . (1975): Chemistry and vegetation of highly acidic streams. - Freshwater BioI. 5: 563- 576. HrLL , B.H. , AT. HERLIHY, P.R. KAUFMANN , RJ . STEVENSON, FH. MCCORMICK & C.B. JOHNSON (2000): Use of periphyton assemblage data as an index of biotic integrity. - J . N. Amer. Benthol. Soc. 19: 50~7 . HrLL, W. (1996): Effects of light. - In: STEVENSON , RJ., M.L. BOTHWELL & R.L.LowE (eds): Algal ecology: Freshwater bentbic habitats: 121-148 . Academic Press , San Diego. HOAGLAND , K.D., S.c. ROEMER, & J.R. ROSOWSKI (1982): Colonization and community structure of two periphyton assemblages with emphasis on the diatoms (Bacillariophyceaea). - Amer. J. Bot. 69: 188-213 . HUDON, C. & E. BOURGET (1983): The effect of light on the vertical structure of epibenthic diatom communities. - Bot. Mar. 26: 317- 330.
From pattern to process
371
HUSTON, M.A. (1979): A general hypothesis of species diversity. - Amer. Naturalist 113: 81-10 I . HUSTON, M .A. (1994): Biological diversity: the coexistence of species on changing landscapes. Cambridge University Press, Cambridge. JONES , J.G. (1974): A method for the observation and enumeration of epibenthic algae directly on the surface of stone. - Oecologia 16: 1-8. KELLY, M.G . (200 I): Role of benthic diatoms in the implementation of the Urban Wastewater Treatment Directive in the River Wear, NE England. - J. Appl. Phycol. 14: 9- 18. KELLY, M.G . & B.A WHITTON (1995): The trophic diatom index: a new index for monitoring eutrophication in rivers. - J. Appl. Phycol. 10: 433-444. KENTUCKY DIVISION OF BIOLOGY (1994): Pond Creek Drainage (Ohio River - Oldham County) Biological and Water Quality Investigation . - Technical Report No. 51. Frankfort, Kentucky. KOLKWITZ, R. & M . MARSSON (1908): Okologie der pflanzlichen Saprobien. - Ber. Deutsch. Bot. Ges. 26A: 505-519. LANGE-BERTALOT, H. (1979): Pollution tolerance as a criterion for water quality estimation. - Nova Hedwigia Beih. 64~ 285-304. LEWIN, J.c. & R.A . LEWIN (1960): Auxotrophy and heterotrophy in marine littoral diatoms. - Canad . J. Microbiol. 6: 127-134. LUTTENTON, M .R. & R.G . RADA (1986): Effects of disturbance on epiphytic community architecture. - J. Phycol. 22 f 320-326. MARGALEF, R. (1960): Ideas for a synthetic approach to the ecology of running waters. - Int. Rev. Gesamten Hydrobiol. 45: 133- 153 . MARKER, A.F.H. (1976): The benthic algae of some streams in southern England. I. Biomass of the epilithon in some small streams . - J. Ecol. 64: 343-358 . MCCORMlCK , P.V. (1996): Resource competition and species coexistence in freshwater benthic algal assemblages. - In: STEVENSON, RJ ., M.L. BOTHWELL & R.L.LoWE (eds): Algal ecology: freshwater benthic habitats: 229-252. Academic Press, San Diego. MEULEMANS , J .T. & PJ. Roos (1985): Structure and architecture of the periphytic community on dead reed stems in Lake Maarsseveen. - Arch. Hydrobiol. 102~ 487-502. MOORE, J.W. (1976): Seasonal succession of algae in rivers. I. Examples from the Avon, a large slowflowing river. - J . Phycol. 12: 342-349. MOORE, J .W. (1977): Seasonal succession of algae in rivers. IT. Examples from Highland Water, a small woodland stream. - Arch . Hydrobiol. 80: 160-171. MOORE, J .W. (1978): Seasonal succession of algae in rivers. Ill. Examples from the Wylye, a eutrophic farmland river. - Arch. Hydrobiol. 83: 367-376. PRECHTL, J ., C. KNElP, P. LOCKHART, K.wENDROTH & U.-G. MAlER (2004): Intracellular spheroid bodies of Rhopalodia gibba have nitrogen-fixing apparatus of cyanobacterial origin. - Mol. BioI. Evol. 21: 1477-1481. PRlNGLE, C.M . (1990): Nutrient spatial heterogeneity: effects on community structure, physiognomy, and diversity of stream algae. - Ecology 71: 905-920 . PRYGIEL, 1. & M. COSTE (1993): The assessment of water quality in the Artois-Picardie water basin (France) by the use of diatom indices. - Hydrobiologia 269/270: 343- 349. ROTT, E., E. PIPP, P. PFISTER, H. VAN DAM ., K. ORTLER., N. BINDER & K. PALL (1999) : lndikationsIisten fUr Aufwuchsalgen in iisterreichischen FlieBgewiissern , Teil 2: Trophieindikation und autiikologische Anmerkungen. -Bundesministerium ftir Land- und Forstwirtschaft , Wasserwirtschaftskataster, Vienna. 248 pp. ROUND, F.E. (1956): A note on some communities of the littoral of lakes. - Arch. Hydrobiol. 52: 398405 .
ROUND, F.E. (1965): The episammon; a relatively unknown freshwater algal association. - Brit. Phycol. Bull. 2: 456-462. ROUND, F.E. (1981): The ecology of algae. - Cambridge University Press, Cambridge . ROUND, F.E. (1991): Diatoms in river water-monitoring studies. - J . Appl. Phycol. 3: 129- 145 . ROUND, F.E . & L. BUKHTIY AROVA (1996): Epipsammic diatoms - communities of British rivers . Diatom Res . 11 : 363-372. SAUNDERS, MJ . & J.W. EATON (1976): A method for estimating the standing crop and nutrient content of the phytobenthos of stony rivers. - Arch. Hydrobiol. 78: 86-10 J.
372
Marian L. Yallop & Martyn G. Kelly
SAY, PJ. & B.A . WHITfON (1975): Chemistry and plant ecology of zinc-rich streams in the Northern Pennines . - In : SAY, P.J & B.A. WHllTON (eds): Heavy metals in Northern England: Environmental and biological aspects: 55-63. University of Durham, Department of Botany, Durham, UK . SLADEEK, V. (1973): System of water quality from the biological point of view. - Arch. Hydrobiol. Beih. 7 (Ergebn. Limnol. 7): 1-218. STEVENSON, RJ . & S. HASHIM (1989): Variation in diatom community structure among habitats in sandy streams. - J. Phycol. 25: 678-686. STEVENSON, RJ . & C.G . PETERSON (1989): Variation in benthic diatom (Bacillariophyceae) immigration with habitat characteristics and cell morphology. - J . Phycol. 25: 120-129. STEVENSON, RJ ., M.L. BOTHWELL & R.L. LOWE (eds) (1996): Algal ecology: freshwater benthic habitats. - Academic Press , San Diego . TUCHMAN, N .C. (1996) : The role of heterotrophy in algae. - In: STEVENSON, RJ ., M.L. BOTHWELL & R.L.LoWE (eds): Algal ecology: freshwater benthic habitats : 299- 319. Academic Press, San Diego . V AN DAM , H . (1982) On the use of measures of structure and diversity in applied diatom ecology. Nova Hedwigia Beih . 73: 97-115. VANNOTE, R.L., G.w. MINSHALL, K.W. CUMMlNS, J.R SEDELL & C.E . CUSHING (1980): The river continuum concept. - Canad. J . Fish. Aquatic Sci . 37: \30-137 . WETZEL, R.G . (1983): Periphyton of freshwater ecosystems. - Dr W. Junk Publishers , The Hague, The Netherlands. WIllTTON, B.A. & DIAZ, B.M. (1981): Influence of environmental factors on photosynthetic species composition in highly acidic waters. - Verh. Int. Vereinigung Theor. Limnol .21: 1459-1465 ZELlNKA, M . & P. MARVAN (1961): Zur Prazisierung der biologischen Klassifikation der Reinheit fliessender Gewiisser. - Arch. Hydrobiol. 57: 389-407. Received 3 March 2005, accepted in revised form 6 October 2005.