hydroecology of river plankton: the role of variability in channel flow

Hydroecology of river plankton: the role of variability inchannel ¯ow

C. S. Reynolds*CEH Institute of Freshwater Ecology, The Ferry House, Ambleside, LA22 0LP, UK

Abstract:The mechanisms by which entrained planktonic organisms survive in river systems, despite an inexorable,unidirectional downstream transport, are revisited. The importance of channel retentivity to downstreampopulation recruitment is emphasized. The aggregated dead-zone (ADZ) model is shown to be adequate to explaindownstream recruitment of a growing population. The ADZ behaviour is more prevalent in sinuous, low-gradientreaches than in other parts of the river. Plankton selection and dynamics relate conspicuously to ¯ow at higherdischarges but other environmental features are important at low ¯ows. Discharge variability is pivotal to theopportunities for potamoplankton to thrive. Copyright # 2000 John Wiley & Sons, Ltd.

KEY WORDS river plankton; channel ¯ow; spatial variability; temporal variability

INTRODUCTION

Whereas the ecology of lacustrine plankton has absorbed the investigative energies of aquatic biologists for

more than a century, its ¯uvial counterpart (potamoplankton) has received only sporadic attention. It is a

fact that most of the knowledge of how planktonic plants and animals have adapted and evolved survival

strategies appropriate to living in suspension has been assembled from observations on lake plankton. The

ecology of marine plankton is far better developed than the ecology of river plankton. Although there may

seem to be few di�culties in transcribing the essential threads from an understanding about resource

gathering, growth and reproduction of individual species and the recruitment and attrition of populations in

standing water to the analogous issues in ¯owing water, there endures a daunting paradoxical problem: how

do microscopic organisms that live their lives entrained in unidirectional river ¯ow overcome the inexorable

tendency to be removed permanently from the river? It is clear not only that they succeed in this but that they

do so with an e�ciency that imparts to rivers a cyclicity of planktonic biomass ¯uctuations that is, broadly,

as regular and reproducible as any annual cycle reported from lakes.

The question has not remained unanswered but the explanations advanced thus far are incomplete in some

important details and the clinching supporting evidence remains tantalizingly elusive. This paper revisits

brie¯y the paradigms and paradoxes relating to the persistence of distinctive planktonic communities in

rivers and updates the hypotheses that appear to explain them. Special emphasis is placed on the

relationships between the dynamics of the plankton and the spatial and temporal variability of channel ¯ow.

The mechanistic evidence required to explain the residence of potamoplankton is restated.

Copyright # 2000 John Wiley & Sons, Ltd. Received 20 February 1999Accepted 27 June 1999

HYDROLOGICAL PROCESSESHydrol. Process. 14, 3119±3132 (2000)

* Correspondence to: C. S. Reynolds, CEH Institute of Freshwater Ecology, The Ferry House, Ambleside LA22 0LP, UK.

POTAMOPLANKTON: THE HISTORICAL BACKGROUND

The persistent occurrence of planktonic organisms in river water was accorded the status of potamoplanktonby Zacharias (1898). Inspired investigations of its composition and periodicity, contributed by Kofoid(1903), Butcher (1924, 1932), Eddy (1931) and Chandler (1937), were among those embodied in Welch's(1952) landmark synthesis. Together with the thoughtful dissertation of Margalef (1960), these authors wereable to fashion a broad understanding of the environmental constraints placed on the growth and survival ofriver plankton, and in devising what Reynolds (1988) termed the `paradigm of the potamoplankton'. Theconsensus had it that successful species required to be pre-adapted to an intensely dynamic environment, tobe sustained from upstream or upcatchment inocula and to be opportunistic in building up populationsbefore they were lost to the sea. It was recognized explicitly that the biomass of river plankton which mightbe achieved was somehow proportional to the age of the water in which it is suspended (Eddy, 1931). Awell-developed potamoplankton would indicate that the water had been in the river long enough for severalplankton generation times to have been accommodated, with a consequent exponential recruitment ofplanktonic biomass: ergo, only long or sluggish rivers were ever likely to support a true potamoplankton(Eddy, 1931).

Subsequent studies have upheld the paradigm. True river plankton, comprising species that are able,without prejudice to the source of their inocula, to increase mass within the riverine ¯ow (Reynolds andDescy, 1996), occurs in larger rivers (third-order streams and greater) throughout the world. In open ¯ow,the number of genera represented in the phytoplankton (mostly diatoms and small green algae) and thezooplankton (often rotifer-dominated) is generally small: that they are also typically able to maintain fastrates of growth, over a wide range of temperatures, is a crucial characteristic of r-selection (Reynolds, 1994).As anticipated, numerous studies have con®rmed that average planktonic biomass typically increasesdownstream (studies reviewed by Rojo et al., 1994), although, in general, only so far downstream as netphytoplankton production is sustainable: in the lower (seventh-order or greater), lowland reaches of thegreat river systems, net phytoplankton production becomes impossible in the severely restricted underwaterlight ®elds (Vannote et al., 1980; Oksiyuk et al., 1990; Wetzel and Ward, 1992). The signi®cant temporal¯uctuations in planktonic biomass are attributable mainly to variability in discharge, although the proximalmechanism relates to the sensitivity of phytoplankton production to the turbidity associated with ¯oodevents, rather than to any acceleration of the ¯ow and the corresponding reduction in the times of travel(Reynolds, 1992).

However, the paradox remains: we are still not quite sure how a plankton remains in a river. Margalef(1960), recognizing that plankton is transported not by strict plug-¯ow but rather, like rinsing a bottle, by aprogressive ¯ushing from the channel, developed the important idea that organisms travel downstream at alesser mean velocity than the water in the main channel. Supposing at least the smaller elements of planktonto be `embedded' in the ¯uid motion of the river (Reynolds, 1997), this itself seems a quite paradoxicalsolution! Margalef's explanation argued, by analogy with the classic deliberations of Riley et al. (1949)about maintenance of gravitating plankton in the vertical, that persistence in the horizontal depended uponthe relative magnitudes of the turbulence generated by the ¯ow (speci®cally, its eddy viscosity) and itsdownstream velocity. As with the Riley solution, it is still necessary for the planktonic organisms to be self-replicating actively for a positive inequality to be maintained; indeed, when realistic velocities and eddyviscosities are substituted, the organismic growth rates required to maintain a presence at a given point in thechannel turn out to be some two to three orders of magnitude greater than the known maximal rates(Reynolds and Descy, 1996, p. 182).

Still more perplexing are the downstream distances in which river plankton can develop. When themaximal populations achieved by planktonic algae in the middle reaches of rivers are compared with theconcentrations of the same species upstream, the supposition may be made that, during transit, the algaincreases in mass, through growth and a series of cell divisions in which each cell divides into two new ones.It is thus a simple matter to determine the minimum number of generations separating the upstream from the

3120 C. S. REYNOLDS

Copyright # 2000 John Wiley & Sons, Ltd. Hydrol. Process. 14, 3119±3132 (2000)

downstream population. When we consider the distance travelled and the speed of downstream transport inthe open channel, we may calculate the apparent time taken to achieve the requisite number of divisions. Astriking instance has been given by Reynolds and Glaister (1993): they observed that the population of thediatom, Stephanodiscus hantzschii, 175 km down the Severn at Buildwas, England, reached 6000 cells mlÿ1,whereas the population at Caersws, only 140 km upstream, never exceeded 0�2 mlÿ1. The increase isnominally equivalent to 15 cell divisions. Supposing an in situ replication rate of one doubling per day (this isthought to be generous; the alga manages about 1�7 dayÿ1 in culture, under constant saturating light at 208C:Hougenhout and Amesz, 1965), for the alga to double every 9�4 km requires that the average downstreamvelocity has to be 5 0�1 m sÿ1. Yet the least velocity measured by Reynolds and Glaister in the open channelof the river at any intermediate station in more than a year was 0�4 m sÿ1. The Severn has several tributariesover this length but these never supplied su�cient inocula to explain the productive excess. No othersigni®cant source of the alga is known. The fact that the phytoplankton may have been simultaneouslysubject to dilution and to losses to sedimentation and to grazers only adds to the paradox.

Reynolds (1995) and Reynolds and Descy (1996) have given several more examples from other rivers inwhich the downstream recruitment is apparently enhanced above that which may be explained by arealistically attainable rate of growth. To varying extents, there is a mismatch among the apparent growthrate of phytoplankton, the distance and velocity of its downstream travel. Either the algal growthperformance exceeds anything accountable from culture work, or the rivers ¯ow further or much moreslowly than is suggested by the channel discharge.

Whatever problem that presents for unicellular phytoplankton, the di�culties are magni®ed formetazoans. Presumably, it is only animals with short generation times that can ful®l the recruitment criteriabefore the river outfalls to the sea. That rotifer species (generation times are sometimes as low as 2�5 days) aregenerally more conspicuous components of river zooplankton than are crustacean plankters (withgeneration times of two to four weeks) may be attributable to their more rapid reproduction.

A further possibility, hitherto considered only cursorily, is that the linkage between upstream anddownstream populations is rather indirect, so that the plankton observed in the river may have charactersdetermined by quite local ¯ow retentivity and which override or, at best, contribute to properties of thewhole river. The following sections seek to reconsider the mechanisms that are hypothesized to explain theparadox and to outline some ®eld campaigns to substantiate them. Later, the contribution of hydraulicengineering of the channel form and the sedimentary refuges are advanced as further in¯uences on the scaleand nature of the dynamics of river plankton, where some revised testable hypotheses are also proposed.

THE IMPORTANCE OF CHANNEL STRUCTURE TO PLANKTON

If the paradox of potamoplankton is to be explained by hydraulic retentivity, it is necessary to demonstrateadequate hydraulic behaviour at the reach scale or less. In general terms, this is not a di�cult challenge. Thesmall-scale velocity structure of a river ¯owing through even a regular, smooth channel is really quitecomplex. Although the anticipated velocity is basically a function of the mass of the water in a reach and theslope down which it is accelerated by gravity, the motion is resisted by friction. The smaller the cross-sectionand the rougher the bed, the more is the potential velocity retarded. Even in larger channels, friction with thesides and bed ensure not only that the ¯ow is unequal through the section but considerable turbulence isgenerated. The detailed complexity in the velocity ®eld is enhanced by longitudinal di�erences in channelform associated with the pool±ri�e sequence and with natural meander sequences. At each added level offocus, the structural variety is enhanced: the examples selected by Carling (1992) convey something of theastonishing variability of the hydraulic transport in natural rivers. Against a steady discharge, water ¯owsthrough di�erent parts of each section at di�erent velocities. These are thus characteristically distributedbetween a maximum, generally only a little (1�2±1�3 times) greater than the mean, down to a minimum,which, except in smooth-surfaced, engineered channels, will be close to zero (see Figure 1).

HYDROECOLOGY OF RIVER PLANKTON 3121


The interpretation of the asymmetric distribution of velocities about the mean is that a part of the channelvolume is ¯owing very slowly indeed or not at all (Day and Wood, 1976). This creates a certain hydraulicretentivity, which impact can be readily estimated from the dispersion of conservative tracers (Valentine andWood, 1977; Bencala and Walters, 1983). If a high-conductivity solute, dye or radioactive tracer is added atone point in the river, then allowed to disperse and ¯ush downstream to pass at least two points whereappropriate (conductivity, ¯uorometric or Geiger) measurements are made, the rate of elution between themcan be calculated. Comparison with normal (Fickian) dispersion models reveals a delay (Figure 2), which isascribed to the retentivity of the channel between each pair of measuring points.

Figure 1. Velocity contours through a cross-section of the River Severn, near Montford Bridge, Shropshire, England, during (a) a lowlate-summer ¯ow, (b) moderate and (c) bankful winter ¯ow. Figure redrawn from Reynolds et al. (1991)

Figure 2. The passage of a pulse of a dissolved marker, injected directly into a ¯owing river, at two separate recording sites furtherdown river, one (trace shown by open circles) `upstream' of the other `downstream' (trace shown by closed circles), compared with theexpected downstream pro®le assuming free Fickian dispersion. The di�erence between the actual and expected downstream readings isattributed to dead-zone retentivity. Figure redrawn from Reynolds (1988), which was based on an original plot in Young and Wallis

(1987)

3122 C. S. REYNOLDS


This behaviour is best explained by visualizing zones of non-¯owing (`dead') water as being ®xed within asteady ¯ow ®eld, Q, but which is continuously and progressively renewed by ¯uid exchange across its shearboundaries. Far from being `dead', in fact, these parts of the ¯ow ®eld represent opportunities for mixingand detention of solutes. Following the development of Young and Wallis (1987), the rate of change inconcentration, c(t), of a conservative solute in any given zone is described by

dc�t�=dt � ÿQ=Vic�t� �Q=Vii�t� �1�

where Vi is the volume of the dead zone and i(t) is the solute input concentration. By analogy, the expressionfor the cumulative impact of a longitudinal series of dead zones can be written

dc�t�=dt � ÿQ=Vec�t� �Q=Vei�tÿ d� �2�

Ve is the aggregate volume of all the dead zones in the reach. The input term is changed to i(tÿ d) torepresent the advective time delay.

Equation 2 thus describes the ®rst-order decay of solute concentration through a river reach, as impactedby the aggregate of its dead zones. With appropriate evaluation of its components, this ADZ (aggregateddead-zone) model has been applied to numerous small- and medium-river channels in north-west England(Wallis et al., 1989). Strikingly, the solution of the immobile fraction, Ve , as a proportion of total reachvolume, falls typically between 0�2 and 0�4. A conclusion which might be drawn is that natural river channelsare not very e�cient at discharging water!

The retentivity of channels through the maintenance of dead zones has very important biologicalconsequences. Clearly, it o�ers a possible mechanism for prolonging planktonic residence, which might helpto explain the potamoplankton paradox. Subject to overriding sinking behaviour and the ability ofsuspended algae to increase their own mass, the control of movements of suspended phytoplankton di�erslittle from that of dissolved tracers. There is also the e�ect on non-living ®ne particles which contribute to theturbidity of river water and, hence, its ability to support underwater photosynthesis. Moreover, thedistribution of ¯ow over the stream bed may also distinguish variation in the grain-size of the bottomsediment and its suitability for occupancy by planktonic consumers and predators.

The most important intellectual question concerns the ability of the dead zones to delay downstreamelution su�ciently to explain the enhanced downstream recruitment of plankton. Crucial to the solution isthe extent to which it is reasonable to treat the ADZ retentivity as a reach character or whether themechanism requires study at a ®ner scale. Recognizing that the dead-zone aggregate includes the boundarylayers adjacent to the river bed and to its banks, eddies behind boulders or fallen trees, the presence ofmacrophyte beds (see, for instance, Dawson and Robinson, 1984), bank-holes, bar-protected shallows on theinside bends of meanders, and natural and anthropogenic blind arms, weir pools and ¯oodplain storages, itseemed important to Reynolds et al. (1991) to investigate the detailed structure of selected reaches in themiddle part of the River Severn, UK. They were able to locate several substantial non-¯owing patches,almost exclusively adjacent to one or other of the banks, often protected by a de¯ecting physical feature (abar, spit, landslip) and visibly separated from the main ¯ow, along a line marked by shedding vortices.Sometimes the protected water would maintain a swarm of Daphnia, the animals gently hanging insuspension and oblivious to the current sweeping past nearby, barely 200 mm away. It turns out that thesestructures are extremely common in this part of the Severn. This was convincingly demonstrated in a latercampaign of airborne remote sensing of the river temperatures: under clear summer skies, the acceleratedheat ¯ux to the river surface continues to be rapidly dissipated into the ¯ow but leads to a rapid warming ofthe water where the motion is weak. There are few more evocative expressions of the patchiness of river ¯owthan the Daedlus thermal line scans of the Severn (see plate 2 of Reynolds, 1995), which distinguisheddi�erences in simultaneous surface water temperatures in the range 16�5 to 218C, in steps of as little as 0�18C,at a spatial resolution of about 1 m. Analysis of the pixel densities from this survey revealed that whereas



some 82±94% of the reach surface was 5 178C, the balance of 6±18% was between 17 and 218C, and aportion (1±4%) was substantially 4 17�58C. The pixel resolution favoured detection of only the largerstorages but these bankside pockets of non-¯owing water, fully veri®able on the ground to be protected byriver bends, bars, macrophyte stands and bank-slumps, occurring with a frequency of 200±300 m, seem likelyto provide the reservoirs of weakly eluting plankton.

Several of the individual dead patches thus located had been subject to earlier studies of their bioticcontents. Using both analogue methods to detect concentrations of chlorophyll epi¯uorescence (as asurrogate of phytoplankton mass) and traditional sampling/counting techniques, we were able to showdisparities between the biomass of phytoplankton within the dead zone and the main ¯ow (Figures 3 and 4).These larger dead zones were persistent between sampling visits, surviving even episodes of bankfuldischarge (Reynolds et al., 1991). The factor of di�erence between the algal concentration in the individualdead-zone and in the main ¯ow varied simultaneously from zone to zone and, for any given zone, fromsampling occasion to sampling occasion. Mostly, the zone-speci®c concentrations observed exceeded thosein the main¯ow by a factor of 1 to 2�5 but some were rather greater. The most remarkable of these was thefan-protected structure identi®ed and veri®ed in the Severn at Leighton Park, Shropshire (NGR: SJ615049;Reynolds et al., 1991; Carling, 1992). A sharp shear boundary separated a non-¯owing or gently-rotatingpatch of water, containing a maximum phytoplankton concentration of 219 mg chlorophyll lÿ1, from a main-¯ow concentration of 5 6 mg lÿ1. Yet more remarkable than the 43-fold di�erence in chlorophyllconcentration was the fact that the dominant alga was of a ¯ushing-sensitive, relatively slow-growing speciesof turbid ponds, Planktothrix agardhii, which had not been detected in the river at all. Despite the physicalcontiguity of the patch with the river, it was obvious that its core was virtually isolated from the ¯ow.

To emphasize its hydrological isolation, this structure was later analogized to `a pond buried in the river'(Reynolds, 1994). It is, however, to be considered a quite exceptional instance of dead-zone behaviour: it is

Figure 3. Fluorimetric pro®les of phytoplankton chlorophyll, from direct measurements in the River Severn in the same section and onthe same three occasions shown in Figure 1. The contour units are quite arbitrary but are relative to the others on the same occasion.

Figure redrawn from Reynolds et al. (1991)

3124 C. S. REYNOLDS


conducive to the understanding of within-river storage but not to the direct explanation of downstreampopulation enhancement. For this to occur, we have to suppose that the water in store is progressivelyexchanged across its shear boundaries with water from the main ¯ow. We also have to recognize that theexchange rate must be compatible with the idea of plankton being in store long enough to raise theirconcentrations, such that the water out may introduce more organisms to the main ¯ow than are present inthe main-¯ow water taken into the dead zone. Clearly, the probabilistic time in store must be comparablewith the organismic regeneration but not so long that the later generations enrich only the dead zone. Theability of the dead zone to maintain an actively increasing population above the concentration exchangedwith the main ¯ow is determined mathematically by the comparative dynamics of population recruitmentand of ¯uid exchange (Reynolds et al., 1991). For a zone of volume Vi , exchanging a volume q hÿ1,containing organisms increasing in number at an average rate of k hÿ1, then the di�erence between theconcentrations inside the zone (Nt) and the input from the main ¯ow (Nf ) is asymptotic to

�Nt�=�Nf� � �q=Vi��

= �q=Vi� ÿ k� � �3�

The asymptote is the point where organismic recruitment through growth just balances the rate of removal inthe exchanged water. Worked examples cited in Reynolds et al. (1991) show how algae increasing at realisticin situ exponential rates of replication of 0�01±0�02 hÿ1 (0�24±0�48 dayÿ1) might maintain realisticconcentrations [15 (Nt/Nf )5 2�5] and still enhance the main-¯ow population (Figure 5).

In order to test the idea that ¯uid exchanges between plankton-maintaining dead zones and the main ¯owmight account for the paradoxically enhanced downstream plankton recruitment at the reach scale,Reynolds and Glaister (1993) proposed a further model. For a given rate of growth over a length of river, the

Figure 4. (a) Spot surface concentrations of phytoplankton chlorophyll and of selected planktonic algae across the transect AA in theRiver Severn at Leighton Park, Shropshire, and just downstream of a fan-like deposit. The contour map (b) is based on a simultaneousremote-sensed false-colour photograph (original in Reynolds et al., 1991) and calibrated from pro®le. Figure redrawn from Reynolds et

al. (1991)



downstream population can be expressed relative to the upstream inoculum (N0). In `plug ¯ow', with nodead-zone retentivity, the downstream population (ND), is assumed to be recruited in proportion to thegrowth rate, such that

�ND�=�N0� � exp�kL=u� �4�

where L is the reach length and u is the mean velocity of the ¯ow. In a reach with a series of dead zones, withan aggregated immobile volume of Ve, we may suppose that Equation 4 adequately describes events in theunexchanged water (1-q/Ve). The enhancement attributable to growth in the exchanged water is given asN0(Nt/Nf )(q/Ve). Combining these components, the downstream population, N*D, is now given by

N�D � N0 �1ÿ q=Ve� exp�kL=u� � �q=Ve��Nt=Nf�

� � �5�

The enhancement attributable to dead-zone behaviour is given by

N�D=ND � �1ÿ q=Ve� exp�kL=u� � �q=Ve��Nt=Nf�

� �= exp�kL=u� �6�

Reynolds and Glaister (1993) used Equation 6 to generate curves to plot downstream enhancement as afunction of aggregate dead-zone volume, Ve , and its net ¯uid exchange rate (q/Ve). The outputs wereanalogized to units of growth per kilometre. Using modest exponents of growth (k � 0�01 hÿ1) and meandischarge velocities of 1 km hÿ1 (c. 0�3 m sÿ1), enhancements of 0�07 kmÿ1 were shown to be theoreticallyachievable. To put this solution into perspective, this is equivalent to accommodating an extra cell doublingevery 10 km that the phytoplankton travels downstream. Thus, reach retentiveness is arguably of amagnitude adequate to explain the `paradoxical' rate of downstream recruitment of Stephanodiscus in theRiver Severn.

It would be satisfying to conclude this section with observational and experimental data to con®rm themechanistic explanation and to overcome its mathematical anomalies. The model ®tted with great success byWhitehead and Hornberger (1984) to chlorophyll data for the River Thames requires the assumption ofYoung±Wallis ADZ retentivity. However, this cannot be taken as proof of the theory. Sad to say, acompelling ®eld demonstration of the hypothesized role of plankton recruitment to river ¯ow from dead

Figure 5. Model reconstructions of the progress to steady-state di�erences in chlorophyll concentration in a dead zone (Nt) relative tothat in the main¯ow (N0), assuming the ¯uid exchange rates shown (q/v, hÿ1) and a constant algal growth rate (0�01 hÿ1; one example

assuming 0�02 hÿ1 is so labelled). Figure redrawn from Reynolds et al. (1991)

3126 C. S. REYNOLDS


zones is still wanting. Working with colleagues on the Severn during the summer of 1995 (one of severedrought), two approaches to veri®cation were attempted. In one of these, the rates at which new cells arereplicated was measured directly in fresh samples of plankton, captured in small containers (`dialysischambers') and circulated mechanically through the vertical depth of selected dead zones; the results werecompared with the observed rates of speci®c population change in the wild river populations (KoÈ hler, 1997).Positive increases in the numbers of cells of Scenedesmus, Chlamydomonas, Cryptomonas and, especially,centric diatoms were found in the containers. Extrapolating from 6 h exposures, the increases inStephanodiscus hantzschii were equivalent to a daily doubling. Replication rates of algae sampled from themain ¯ow and from the dead zone were statistically indistinguishable. They were always greater than those ofthe same species in non-circulating controls and were also much greater than the rates of change in the openwater of the dead zone: far from increasing, the standing crops of diatoms actually decreased. KoÈ hler (1997)attributed this large shortfall in natural performance to the sedimentation and (mainly benthic) grazinglosses that the dialysis chambers prevent. This may seem implausible but it is not at all uncommon to ®ndnegative controls detracting from the realization of phytoplankton biomass in rivers during summer(Reynolds and Glaister, 1993; Gosselain et al., 1994; Reynolds, 1995); in this instance, if the proposedmechanism of downstream enhancement was active, it was exceeded by the impacts of in-channel losses.

The second approach attempted to emulate the method devised by de Ruyter van Steveninck et al. (1992)who followed, quite literally, the development of a phytoplankton along the length of the River Rhine, bysampling what they took to be the same parcel of water with which their boat drifted downstream. Supposingthe downward-drifting water parcel to be, in fact, subject to persistent exchanges with slow- or non-¯owingwater, our design sought to relate downstream plankton recruitment to the presence of local dead-zones withveri®able population pockets along the river course. In the ®rst attempt, in July 1995, we sampled from aboat drifting with the natural ¯ow, between Cressage and Buildwas on the Severn (9�5 km were covered in 7�5h). Disappointingly, the phytoplankton biomass (`dominated' by the chlorophyte Scenedesmus) remainedstubbornly low throughout; the known dead zones, with directly veri®ed elevated surface temperatures (inone case, over 288C, and around 98C warmer than the main¯ow), supported dense stands of Enteromorpha, anon-planktonic alga, and with no signi®cantly elevated concentrations of river phytoplankton.

No evidence of downstream enhancement of the plankton population was forthcoming on this occasion.Undaunted, another campaign was undertaken in August, this time working a higher section of the Severnwhere Enteromorpha stands were less prevalent (Crew Green±Montford: 17 km). A net downstream loss ofbiomass of centric diatoms was again observed and, although there was a small net recruitment of greenalgae, the observed increase was not demonstrably reliant on the dead-zone exchanges. On this occasion,however, the dialysis chambers were simultaneously circulated in the main ¯ow as the boat drifteddownstream. These showed a strong positive increase in the numbers of Scenedesmus (10�3% hÿ1) and ofStephanodiscus (16�9% hÿ1: see KoÈ hler, 1997) in water freshly sampled from the river. The results cannot besafely extrapolated to the full 24 h: the provisional calculation of in situ replication rates su�cient to doublethe green algal population in c. 7�1 h of those of the diatom to do likewise in under 4�5 h is not authenticable.Nevertheless, it is interesting to note that, travelling downstream at just under 0�3 m sÿ1, the observedincreases translate to distance-speci®c increase rates equivalent to 0�092 kmÿ1 for the Scenedesmus (adoubling every 7�5 km) and 0�147 kmÿ1 for the Stephanodiscus (doubling every 4�7 km).

On this basis, it would be possible to explain all cases of enhanced downstream recruitment of planktonyet observed, without needing to invoke the presence of dead zones. Nevertheless, even when allowance ismade for the higher water temperatures and irradiance levels obtaining, the extrapolable planktonreplication rates exceed the performances of cultures in the laboratory (see above). Setting aside thatanomaly, the fact that the algal populations increased so little in the river itself demands the assumption ofrates of cell loss equivalent to population halvings every 4±8 km. To lose diatoms faster than green algae,especially when the water depth is low, is not unexpected (Reynolds et al., 1990), neither is the fact that lossescould exceed recruitment by replication (data of Gosselain et al., 1994; see also Lair et al., 1998). However,the scale of losses required to o�set rates of recruitment, even substantially lower than the provisional



measurements here serve only to renew a sense of ignorance about the extent of loss processes in rivers andtheir coupling to plankton anabolism.

THE IMPORTANCE OF CHANNEL VARIABILITY AT THE BASIN SCALE

The study of potamoplankton recruitment in the Rhine by de Ruyter van Steveninck et al. (1992) has beeninspiring for other reasons too, not least for its reconstruction of the spatial and temporal dynamics ofdevelopment at the scale of a major part of the river basin. The results from the separate downstream cruiseswere seasonally distinguishable (they also experienced poor downstream recruitment in summer), the mostoutstanding performance being that detected in May 1990. Over the 233 km between Maxau and Koblenz,the phytoplankton population increased by the equivalent of 3�3 doublings (one doubling every 70 km).Given the spring conditions of low temperature and relatively high discharge (sustaining a mean velocity of0�837 m sÿ1), the downstream recruitment (0�0097 kmÿ1) still requires an impressive rate of cell growth (0�70dayÿ1 or, roundly, a biomass doubling per day). It is evident from the contemporaneous determinations ofphotosynthetic capacity, presented in de Ruyter van Steveninck et al. (1992), even when corrected for theturbidity of the river and the hours spent in darkness, that an average aggregate of 5 h of light-saturatedphotosynthesis each day would sustain such a rate of growth. Again, the outcome is not intuitively expected:maximum rates of net population increase for planktonic algae in other rivers, estimated from literature datareviewed by Reynolds and Descy (1996: values of 0�23±0�43 dayÿ1, equivalent to one division every secondor third day), generally invoke a slower rate of replication to underpin the reported downstream recruitment.The possibility that exchanges involving dead zones could have contributed to the observed recruitment is inno way invalidated but there is no clear evidence that such mechanisms were functional, neither is there amathematically sustainable argument that they should have been.

In a study of phytoplankton growth in a series of British rivers, Reynolds (1995) compared measuredincrements of biomass of key algal species over selected reaches with the increments predicted by modelequations expressing algal replication rates as a function of temperature and aggregate daily photoperiod(Reynolds, 1989), against habitat descriptions for each reach considered at each of three seasonal samplings.The rationale was that the excess of actual growth performance over conventionally anticipated growthpotential would provide a statement about the hydraulic behaviour in the river reach in question. Forexample, the model equations might be used to predict that, in clear water under equinoxial insolation and ata temperature of 108C, Scenedesmus coenobia should increase at the rate of 0�21 dayÿ1. If the measuredvelocity at an upstream site is (say) 0�5 m sÿ1, then the same main¯ow water parcel would take 6 h to reach anext point of measurement, 10�8 km downstream, by which point the Scenedesmus population could beexpected to have increased by not more than the equivalent of 0�0525 (i.e. by 5�4%). Indeed, allowing forsinking and grazing losses, a rather lower increase could, quite reasonably, be anticipated. In fact, as claimedearlier, the observed downstream populations had frequently been augmented by a signi®cantly greaterpercentage. By back-calculation, a speci®c rate of increase was derived for each main species. Thesupposition was then made that the di�erence from the model calculation is attributable directly to thee�ects of a delay in the time of travel and the factor of di�erence is at least coarsely scaled to reach retentivity.In this way, the recruitment performances of these algae become, as it were, live markers of aggregated dead-zone behaviour along the river.

The results of this study are summarized in Reynolds (1995). These showed contrasts between river basins,most particularly with respect to the distances travelled, average bed gradient and sinuosity (how much theriver is distorted from straight descent of its valley). Not only were the greatest accumulations of plankton tobe demonstrably in the low-gradient reaches of rivers such as the Severn, Thames, Trent and Great Ouse butthe exaggerated rates of downstream appreciation were con®ned to sections with mean gradients of 5 0�5 mkmÿ1. There were also large di�erences in the plankton supported at di�erent times of the year. The largestbiomasses were observed during April 1991, when diatoms, usually species of centric genera (Stephanodiscusand Cyclotella), were relatively abundant in most of the rivers examined. Multiple regression analysis also

3128 C. S. REYNOLDS


showed a statistically signi®cant ®t of population recruitment to river gradient and sinuosity. In other words,the behaviour of the respective plankton communities proved an adequate, if noisy, discrimination of theriparian characteristics and channel ¯ow patterns represented across the spectrum of the 18 British riversselected for the survey. In June 1990, under conditions of declining ¯ows, plankton composition was morevariable and downstream enhancement of recruitment was less strong and less consistent (regression againstsinuosity and gradient were just signi®cant at the p5 0�05 level). Analysis of the comparable data set for theSeptember 1990 sampling found the greatest idiosyncrasies in composition and abundance and very poorcommonality of behaviour with respect to the basin characters. No statistical correlation was found todescribe between-river and between-reach variability.

The spring and early summer results are shown in Figure 6. The contours are generated from the respectivemultiple regression equations to show the survey-wide seasonal di�erences in channel ¯ow. These have beeninterpreted as follows. That the plankton behaviour is so clearly correlated to river form in spring isattributed to its regulation primarily by relatively high discharge and its correlated constraints (especiallyturbidity). At such times, retentive structures, including dead zones and signi®cant pool reaches, exert anoverriding in¯uence upon downstream recruitment: without retentive refuges, all recruitment must takeplace in open ¯ow. Relatively high velocities, signi®cant turbidity and low temperatures contrive to increasethe hostility of the environment to plankton development and thus accentuate the contribution of processesful®lled in the regions of impeded ¯ow.

Under conditions of lower ¯ows, longer days, warmer temperatures and clearer water, these physicalconstraints are eased and the plankton responds to more familiar controls. Potentially, algal biomass canincrease exponentially, to limits set by the nutrient capacity or the underwater light availability. Equally, the

Figure 6. (a) Retentivity-enhanced phytoplankton recruitment in some British rivers during June 1990 as a function of reach gradientand sinuosity. The ®tted multiple-regression contours link points predicted to support the enhancement to apparent growth rate, r(units, kmÿ1). (b) The equivalent contours ®tted to data for the same set of rivers, during relatively greater discharges, in March±April

1991. Figure redrawn from Reynolds (1995)



biomass may become quickly subject to chemical (carbon exchange and nutrient supply) or biotic (grazing,including or especially by benthic consumers) controls, exceeding in importance the hydraulics of the river.Mainly, these are not properties owing to channel form: the development of the plankton is uncoupledprogressively from regulation by the constraints of channel ¯ow.

It is arguable that, in general, it is the rapid generation times of planktonic algae that enable them tosurvive the seemingly hostile conditions in rivers and to exploit the opportunities that the physical respite oflow ¯ows brings. For the planktonic animals of the river, the survival and exploitative opportunities arerelatively diminished, simply because their generation times are longer and the opportunities arecorrespondingly truncated. It would seem that ¯ow variability would exert direct impacts on the abundanceand composition of zooplankton.

In a recent comparison of zooplankton structure and dynamics in some representative European rivers,Viroux (1997) has shown, very elegantly, that the time of travel normally does not allow much time for asigni®cant zooplankton to develop, save for the rotifers, such as Keratella and Brachionus and, perhaps,protists, including Di�ugia, Coleps and Tintinnidium, whose rates of population increase approach those ofthe algae. Thus, in many short to medium rivers, exempli®ed by the Meuse, rotifer species are likely toconstitute the dominant zooplankton, usually in episodes promoted by the abundance of small planktonicalgal foods. Crustaceans are rarely abundant in the Rhine but in a less trained, more natural river, dead-zoneretentivity can create refuges and buy time for the recruitment of successive generations: Viroux showscladocerans and copepods to be very much more conspicuous in the plankton of the Moselle.

As indicated above, cropping of river phytoplankton is not an opportunity exclusive to zooplankton:systematic studies are needed to substantiate the conjecture that, in soft-bottomed low-gradient rivers, themajor consumers of planktonic algae may be benthic chironomids or ®lter-feeding lamellibranchs(Reynolds, 1988). Consumption rates would be subject to food supplies, consumer concentration andwater temperature but would not have to depend upon a consumer recruitment response: a large populationof feeders could be in existence before an algal bloom became established. In this way, the nature of thesecond trophic level of plankton-bearing rivers is seen to be closely related to the hydrology of the river, mostespecially through the interaction of geomorphology and ¯ow variability, and subject always to theanthropogenic modi®cations to channels and hydraulic regulation.

CONCLUDING DISCUSSION: IMPACTS OF FLOW VARIABILITY IN THE ECOLOGY OFPOTAMOPLANKTON

Uncertainties persist about the mechanisms governing the ecology of potamoplankton. For many, nutrientconstraints occupy the same central place in the understanding of the dynamics of river plankton that theyare supposed to do in lakes (see, for instance, Basu and Pick, 1996). As is true of lakes, the size of the resourcebase sets a supportive capacity which regulates the upper level of plankton biomass that could be carried.This can be compared with capacites set by, for example, underwater light availability, or the e�ciency ofdownstream transport. Again as in lakes, large phytoplankton biomass cannot be generated without aplentiful supply of nutrients, neither can a modest supply ever support more than a modest biomass. Neitherstatement precludes the possibility that biomass can be low when nutrients are abundant, simply becauseother factors exert greater constraints.

In rivers, these other constraints may well be operative, not to say overriding, at certain and substantialtimes of the year. They certainly include episodes of high discharge, when plankton is transported quicklyseawards, embedded in a medium rendered so turbid by entrained ®ne particulate matter (clay and silt, aswell as biogenic material) that net population increase is impossible owing to light deprivation. Theanalogous argument to the last sentence of the previous paragraph may be invoked: large phytoplanktoncrops cannot be generated under conditions of high ¯ows and its associated elevated turbidity levels but,equally, large populations can be resisted under low ¯ows by modest inocula, rapid grazing or sedimentarylosses and, especially, by a shortage of nutrients.

3130 C. S. REYNOLDS


Most rivers are subject to frequent variability in discharge and, hence, in discharge-sensitive attributes ofthe biotic environment. There is a ¯uctuating plankton-carrying capacity and very often there is a timeconstraint upon the exploitation of the opportunity before the capacity is altered (either through reneweddischarge limitation or supersedence of chemical constraints) or its achievement is prevented biotically. It islittle wonder that the attributes of the relatively few types of planktonic organism that are successful in riversare so conspicuously exploitative and opportunistic (r-selected properties: Reynolds, 1994). Once thedownstream-transport constraint is alleviated, other events may transpire, other respondents enter thepicture, other factors become limiting. The override of ¯ow is so weakened that other ecological factorsassume greater importance. The plankton behaviour ceases to be governed by tangible, quantitativerelationships to ¯ow.

In spite of this, certain selective biases of ¯ow will persist. The planktonic performances, both indownstream recruitment and in forming large biomasses, remain impressive and are still incompletelyexplained. Inocula still need to be present and their responses still have to be prompt if the opportunities areto be exploited, whenever the discharge constraint is weakened. It seems the hypothesis concerning theaggregated dead zones and the channel-dependent retentivity that these may provide has not beeninvalidated. In addition, the source of opportunity-exploiting inocula is also likely to involve recruitmentfrom within-river refuges. These include the ¯oodplain and, signi®cantly, the river sediment and the surfacesof channel macrophytes. Meroplankty, the ability to pass part of the life cycle out of the ¯ow, is stillhypothesized to contribute to the narrowness of the range of genera that are able quickly to turnopportunities into dispersive population events (Butcher, 1932; Reynolds and Descy, 1996). Bothmechanisms remain insu�ciently investigated; for the present, neither of the hypotheses has beeninvalidated.

Even without this detail, existing knowledge permits an unconditional recognition that the dynamics ofriver plankton are very responsive to the variations in channel ¯ow. Nevertheless, there is no continuous,linear relationship, in the sense that discharge can be used to predict the plankton biomass. Rather,increasing ¯ow imposes quanti®able constraints on planktonic development and which quickly achievecritical and decisive proportions. Decreasing ¯ow allows control to pass to other constraints. Thus therelationship of plankton to ¯ow is, e�ectively, inactivated. However, it is the temporal ¯ow variability thatregulates the opportunities for the potamoplankton to react to them and to contribute to the economy of theriver system.

ACKNOWLEDGEMENTS

I am grateful for the invitation of the editors to write this article. I feel privileged to be considered able to doso, mainly on the strength of past collaborative studies undertaken with the support of the (then)Department of the Environment and the (then) National Rivers Authority. These studies involved numerouscolleagues, most notably, Dr Paul Carling and Mark Glaister, formerly of my Institute, Professor KeithBeven and his group at the University of Lancaster. They led to subsequent collaborations with Dr JanKoÈ hler, of the IGB in Berlin, and Dr Jean-Pierre Descy, of FUNDP in Namur, whose insights andenthusiasms have in¯uenced this account. I am very grateful to my colleague, Dr Tony Irish, and for hisvaluable assistance in generating the ®gures in this account.

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hydroecology of river plankton: the role of variability in channel flow

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