FORUM is intended for new ideas or new ways of interpreting existing information. Itprovides a chance for suggesting hypotheses and for challenging current thinking onecological issues. A lighter prose, designed to attract readers, will be permitted. Formalresearch reports, albeit short, will not be accepted, and all contributions should be concisewith a relatively short list of references. A summary is not required.

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Changes in community properties during microbial succession

Colin R. Jackson, Dept of Biological Sciences, SLU 10736, Southeastern Louisiana Uni�., Hammond, LA 70402,USA (cjackson@selu.edu).

Succession is one of the oldest concepts in communityecology and various theoretical and empirical studieshave addressed succession and it’s underlying mecha-nisms, particularly in plant communities (Odum 1969,Connell and Slatyer 1977, Finegan 1984). The develop-ment of algal periphyton on submerged rocks instreams has also been viewed as an example of succes-sion in autotrophic communities (Stevenson 1983,Johnson et al. 1997). More recently, the formation ofbacterial communities on submerged surfaces (biofilms)has been viewed in the context of primary ecologicalsuccession (Jackson et al. 2001), and studies have usedmolecular techniques to examine the changes in bacte-rial community structure that occur during biofilmdevelopment (Santegoeds et al. 1998, Jackson et al.2001). Briefly, when a fresh surface (glass slides, rocksetc.) is submerged in an aquatic habitat it is rapidlycolonized by bacterial populations, some of which willgrow and persist as part of the attached biofilm com-munity. These initial heterotrophic populations are de-pendent upon the availability of dissolved organiccarbon (DOC) from the overlying water, i.e. it is anopen system with little internal cycling of nutrients orcarbon. Over time, new populations of bacteria arrivethrough immigration from the water column, whereasother populations are lost from the community, eitherthrough cell death and losses due to sloughing, orbecause conditions in the biofilm change (largely be-cause of microbial activity and growth) and those bac-teria are no longer adapted to biofilm life. The lattercase recalls the facilitation model of Connell andSlatyer (1977) in that early colonizing bacteria changethe environmental conditions in the biofilm, facilitatingthe later dominance of different populations (indeed,those authors suggested that the facilitation mechanismmay be particularly applicable when organisms arecolonizing a new substrate, i.e. during primary succes-sion, which is likely to be the case during biofilmformation). In the later stages of biofilm development,populations of heterotrophic bacteria are more depen-

dent upon autotrophic production occurring within thebiofilm (such as from algae or cyanobacteria), i.e. thecommunity becomes more of a closed system.

Based on the results of a recent study of epilithicbiofilm development, Jackson et al. (2001) suggestedcertain conceptual changes that might occur in commu-nity properties during bacterial biofilm succession (Fig.1). Initial colonization of a fresh surface leads to arapid increase in species richness (S), which subse-quently declines as some of the colonizing populationsare less competitive and do not survive in the biofilmcommunity. However, competition becomes less impor-tant in structuring the bacterial assemblage as the bi-ofilm ages and new resources and habitats becomeavailable (such as through the accumulation ofmetabolic waste products that can serve as growthsubstrates for other organisms, the emergence of anoxicpockets permitting the growth of anaerobic bacteria,and the development of a three dimensional architec-ture allowing greater area for attachment and growth).Thus, S might increase again as the biofilm communitymatures, and community structure is driven by resourcediversity rather than by competition. This model canhowever be extended, and a number of changes madeto more accurately explain community changes.

Firstly, the term resource diversity is vague. Origi-nally the increase in resource diversity throughout com-munity development was intended to convey both theappearance of new substrates for microbial growth, anda switch from a two dimensional community to a threedimensional one (so an increase in both habitat spaceand variety). An alternative term would be the numberof ecological niches, and what was originally describedas an increase in resource diversity can be more suc-cinctly thought of as an increase in the amount of nichespace (R, following MacArthurs’ (1972) idea of a re-source spectrum, and assuming that resource spectrumlength is equivalent to niche space). Thus, as the biofilmdevelops, the increased heterogeneity of the communityfacilitates a continuous increase in the potential number

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Fig. 1. Summary of the conceptual model suggested by Jack-son et al. (2001) for changes in community properties thatoccur during bacterial biofilm succession. Early biofilms showrapid colonization by many populations, resulting in increasedcompetition in mid-development biofilms, which depressesspecies diversity. An increase in resource diversity duringbiofilm development lessens the affect of competition andpromotes an increase in species diversity in more maturecommunities.

Fig. 2. A revised model of the changes in community proper-ties that occur during bacterial biofilm succession. Speciesrichness (S) increases because of initial colonization by manybacterial species, but declines as competition for broad-scaleresources (such as space) begins to structure the community.The transition from a two-dimensional habitat to one ofthree-dimensions, coupled with the increase in substrates avail-able for growth results in an increase in niche space (R),facilitating a second increase in richness. As the communitymatures, more specialized populations using specialized re-sources causes a shift from broad-scale competition to compe-tition at a finer scale, within particular functional groups.Because R continues to increase, new species (Sn) are added tothe community, even on the later stages of succession. Inmature communities, the number of new species added overtime will tend to stabilize (if R increases linearly, solid line) orincrease (if R increases geometrically, dashed line).

of niches. While the potential number of species shouldtherefore increase throughout biofilm development, inactuality S is depressed during the early-middle stagesbecause sufficient additional niche space has not yetaccumulated to accommodate the additional species.Thus, some of the early colonizing populations are lostthrough competition (Fig. 2). In essence, the first peakin species richness in the model of Jackson et al. (2001),and observed experimentally in that study and the oneof Santegoeds et al. (1998), represents the initial pres-ence of more populations in the community than cancurrently be supported. Thus, competition serves tostructure these early-middle aged communities, but maybe less important in later stages.

The concept of competition in biofilm communitieswas poorly developed in the original model. Withinbiofilm assemblages, competition must be examined at

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two levels of resolution: what we can think of as broadscale competition that influences all organisms in thecommunity (for example, competition for space on thesubmerged surface, or for resources required by themajority of populations), and as fine scale competitionfor resources that are only needed by certain bacterialpopulations (for example, oxygen is only needed byaerobic populations, or sulfate is primarily required bysulfate-reducing bacteria). The previous successionmodel focuses solely on competition at the broad scale,which was reasonable given that in early and middleaged biofilms much of the competition will likely be forgeneral resources and space needed by all populations.However as S and R increase, increased numbers ofspecialized populations will require more specific re-sources; thus competition at a fine scale should increasein the later stages of biofilm succession. In consideringthe initial stages of biofilm formation, this fine scalecompetition is also likely to be important, not becauseof large numbers of specialized bacteria, but becausespecific resources are in very scarce supply. So fine scalecompetition should initially be high (limiting specificresources), decline (increased resources), and then in-crease once more (increased numbers of populations)over the course of community development. Essentially,we may see switches between fine scale and broad scalelevels of competition as a structuring force (Fig. 2).

Demonstrating that these changes in communityparameters occur is difficult. Jackson et al. (2001) wereable to show the general changes in S during develop-ing bacterial biofilms using molecular techniques (spe-cifically, denaturing gradient gel electrophoresisexamination of 16S rDNA fragments, where separatebacterial populations are assumed to produce distinctbands in gels). An earlier study by Santegoeds et al.(1998) used similar techniques and similar patterns in S(initial increase, followed by a decrease, and later in-crease as the biofilms matured) were apparent. Examin-ing the data (gels) obtained in these studies suggestsanother parameter that might support the predictedpattern of biofilm community succession: the number ofnew species (new bands) appearing at each stage. Giventhat R should continually increase, it would be expectedthat following an initial decline (the appearance of newspecies must initially be high because of colonizationand community formation), the number of new species(populations that have not been detected in the commu-nity prior to that date; Sn) that are added to thecommunity should either remain constant (if R in-creases linearly) or increase (if R is increasing at a rateapproaching exponential; Fig. 2). This is assuming thatS is still increasing in the later stages of succession (i.e.the addition of new populations represents a net gain tothe community, not simply the replacement of onepopulation by another). Given that both Santegoeds etal. (1998) and Jackson et al. (2001) reported increases inS in the later stages of biofilm development, the contin-

ued appearance of new populations in these biofilmswould strongly support the notion that R is increasing.Essentially, the appearance of new populations couldbe used as an indirect measure of new niche space.

The two studies were conducted over similar periodsof time (84 d for Santegoeds et al. 1998, and 90 d forJackson et al. 2001) and used comparable techniques(both identified species richness by counting the num-bers of distinct bands in gels, and both comparedcommunity structure by examining changes in bandingpatterns over time). Jackson et al. (2001) used glassslides as a surface for bacterial growth, whereas Sante-goeds et al. (1998) used plastic foil. Santegoeds et al.(1998) submerged a single set of surfaces in an activatedsludge treatment basin (and so followed the develop-ment of one set of biofilms) while Jackson et al. (2001)followed two sets of biofilms in a wetland mesocosmand an additional set submerged in a small lake. Bothstudies described changes in species richness that fit thepattern of the biofilm succession model. Re-examiningthe gels obtained from each study and focusing on theappearance of novel species also shows similar patternsbetween all four sets of biofilms (Fig. 3). In each casethere is an initial decline in Sn in the early stages ofcolonization, but new populations continue to appearthroughout community development (Sn even increasesin later activated sludge biofilms suggesting that R isincreasing rapidly). Thus, the observed patterns in theappearance of new species in various sets of biofilmsseem to fit the prediction suggested by Fig. 2: that Snshould remain constant or increase, suggesting increas-

Fig. 3. Changes in the number of new populations (Sn) de-tected in bacterial communities at different time points duringfour biofilm succession experiments. New populations wereinferred from the appearance of novel bands in denaturinggradient gel electrophoresis gels. Biofilm communities repre-sent those examined by Santegoeds et al. (1998) from anactivated sludge reactor (solid triangles), and those from a lake(squares), and a wetland mesocosm (two sets: open trianglesand circles) examined by Jackson et al. (2001). Patterns in Snresemble those predicted by the conceptual model in Fig. 2.

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ing values of R, or greater resource diversity and nichespace as the biofilm community matures.

In summary it seems that a number of predictionscan be made about the successional changes that occurduring the formation and development of bacterialbiofilm communities. S increases initially because ofrapid colonization, but is then reduced as some earlycolonizing populations cannot compete for space andother broadly needed resources and are excluded fromthe community. However, as the community developsthere is an increase in the potential number of niches,combined with the appearance of more specialized pop-ulations. Thus, an increase in R promotes a secondincrease in S, and competition becomes more of astructuring force at a finer level for more specializedresources. Because R continues to increase (with in-creasing habitat heterogeneity), new species continue tobe added to the community as new niches becomeavailable, although at some point both R and S muststabilize. In some general ways, microbial biofilm com-munities may fit exploitation models of ecosystem for-mation, whereby increases in production at one trophiclevel facilitate the development of higher trophic levels(Oksanen et al. 1981). However, with regard to bacte-rial biofilm communities the initial trophic level mightnot consist of autotrophic organisms, but might consistof heterotrophs utilizing organic carbon from outsidethe system (DOC in the water column). These initialpopulations could act as a source of nutrition (by theproduction of waste products, for example) for laterorganisms, which could certainly be viewed as differenttrophic species if not a different trophic level. Indeed,the concept of trophic levels is difficult to apply tobacteria given that primary production can occurthrough both photosynthesis and chemoautotrophy,and that many of these organisms are also capable ofheterotrophic nutrition (i.e. they are mixotrophs). Evenin simplified microbial systems, with algae andcyanobacteria serving as a source of carbon for hetero-trophic bacteria, trophic pathways are likely to benon-linear, with exchange of nutrients (and potentiallycarbon) in multiple directions.

It is likely that in the later stages of biofilm succes-sion, trophic interactions between bacteria and otherorganisms become more prevalent, and top-down con-trol through factors such as predation (by protists, orby biofilm grazing macroorganisms such as snails) orviral lysis may be more important than resource diver-sity and competition in structuring the bacterial com-munity. Little is known about how such factors mightaffect bacterial community properties, particularly inbiofilms. It could be argued that predation might sup-press bacterial numbers and drive down S (and also R,if we accept that some niches arise from the activity ofcertain bacterial species), however there are classic ex-amples with larger organisms where predators selec-tively prey on certain populations, and can result in

increases in diversity through the suppression of supe-rior competitors. Indeed, it has been observed thatsome protist predators preferentially remove larger bac-teria from pelagic communities (Simek 1992) and itcould be argued that larger bacteria are larger becausethey are better competitors. Whether such things astrue protistan ‘‘keystone species’’ (Paine 1966) exist formicrobial communities remains to be seen. Regulationof bacterial populations by viral lysis is undoubtedlyspecific given the nature of the viral–host interaction,and recent models suggest that coexistence of compet-ing bacterial populations might be maintained throughincreased viral lysis in larger (and presumably morecompetitive) bacterial populations (Thingstad 2000).Thus, as the biofilm matures, a switch from bottom-upcontrol through niche diversity and competition totop-down control through predation and lysis is likelyto occur.

While these predictions apply specifically to attachedbacterial communities, similar patterns might be seen incommunities of other organisms. Increased resourceand habitat heterogeneity must be a driving factor inthe primary succession of any taxonomic group (R inany new habitat must be low, and must increase follow-ing colonization as early colonizing organisms modifythe habitat). Similarly, increases in species richness havebeen observed in the succession of various communities(an initial increase in S must happen if it is initiallyzero) and a subsequent decrease in richness is likely aresult of a trade-off between colonization ability andcompetitiveness, which in biofilm communities is less-ened as new niches become available. Resource-ratiomodels of plant succession (Tilman 1985) emphasize therole of competitive interactions in shaping communitystructure, but generally focus on competition for alimited number of resources (what might be thought ofas the broad scale competition described above). Suc-cessional models for microbial communities should fo-cus on competition for resources that are needed by allcommunity members and those that are just requiredby certain populations. It should be remembered thateven the most complex plant community is simple bymicrobial standards, in that all of its populations re-quire the same basic resources and function in the sameway. Microbial communities are diverse assemblages atboth taxonomic and functional levels. They may con-tain prokaryotes and eukaryotes, autotrophs and het-erotrophs, aerobes and anaerobes, all of which may beoperating in different ways, requiring different re-sources. Because they are so complex, the analysis ofmicrobial communities is far behind that of plant oranimal communities, and there is little experimentalevidence from which to predict phenomena such asecological succession. However, by incorporating andmodifying theories developed for other taxa, microbialecologists can begin to establish the theoretical frame-

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work necessary to predict spatial and temporal patternsin the structure and functional of microbial communi-ties.

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