A Physiological Interpretation of the Dynamic … · A Physiological Interpretation of the Dynamic...

A Physiological Interpretation of the Dynamic Responses of Populations of a PlanktonicDiatom to Physical Variability of the EnvironmentAuthor(s): C. S. ReynoldsSource: The New Phytologist, Vol. 95, No. 1 (Sep., 1983), pp. 41-53Published by: Wiley on behalf of the New Phytologist TrustStable URL: http://www.jstor.org/stable/2434170Accessed: 13-02-2017 19:22 UTC

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New Phytol. (1983) 95, 41-53 41

A PHYSIOLOGICAL INTERPRETATION

OF THE DYNAMIC RESPONSES OF POPULATIONS

OF A PLANKTONIC DIATOM TO PHYSICAL

VARIABILITY OF THE ENVIRONMENT

BY C. S. REYNOLDS

Freshwater Biological Association, The Ferry House, Ambleside, Cumbria, LA22 OLP

(Accepted 21 April 1983)

SUMMARY

The dynamic responses of Fragilaria crotonensis populations to artificial variations in the mixed depth of the water column of a Lund Tube (Enclosure C, Blelham Tarn) are shown to conform to a descriptive model involving only two environmental variables: mixed depth and optical depth. The physiological interpretation of these responses invokes a second model, relating the rates of net population change to photosynthetic productivity, corrected for respiration, and to in situ sinking loss rates. Population increases coincide with mixing episodes, when it is shown that the maximum photosynthetically-derived growth rate exceeds the sinking low rate by an amount similar to the observed rate of net gain. Abrupt declines occur when the column rapidly

restratifies, at rates explicable in terms of accelerated sinking and sinking-loss rates, i.e. that there is also an abrupt cessation in growth. Evidence that this effect is due to extreme near-surface photoinhibition is presented. The ecology of Fragilaria populations is briefly discussed in relation to these findings.

INTRODUCTION

There have been numerous attempts to relate the population dynamics of freshwater phytoplankton to their photosynthetic productivity. These have been extensively reviewed by Harris (1978): the various physiological processes involved - photosynthetic rate, respiration, photoadaptation, photoinhibition and intracellular assimilation of photosynthate - react in different ways to temperature, the duration, intensity and relative penetration of solar irradiance and to the often overriding effects of turbulent motion. Moreover, it seems clear that different species of phytoplankton from different aquatic environments do not respond in identical ways. Not surprisingly, then, few generalizations about phytoplankton population dynamics, based upon models of photosynthetic productivity, are currently available.

In this paper, the relationship is approached from an opposite standpoint: known changes in the standing population of a planktonic diatom, Fragilaria crotonensis Kitton, in a large, limnetic enclosure ('Lund Tube' C, Blelham Tarn, English Lake District) during a single, 'summer' period (May to September, 1982) are compared with model predictions of the maximum photosynthetic productivity, subject to artificially-imposed variations in the physical characteristics of the environment. Several contributory factors suggested that such an approach might be profitable. First, Fragilaria is a non-motile diatom whose distribution, both in space and in time, is influenced by the extent and duration of turbulent mixing processes (Reynolds, 1980; Reynolds et al., 1982, 1 983b). Second, recent experience

0028-646X/83/090041 + 13 $03.00/0 (? 1983 The New Phytologist


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42 C. S. REYNOLDS

has established that measurements of changes in the standing populations of planktonic diatoms in the Lund Tubes can be made with reasonable precision

(Reynolds et al., 1982). Third, these same systems can be conveniently manipulated to maintain selectively favourable environments for particular species of phytoplankton (Lund and Reynolds, 1982; Reynolds et al., 1983b). Fourth, that in contrast with many species of algae, there is supposedly a good correlation between growth and photosynthetic behaviour among planktonic diatoms (Talling, 1955, 1957a, b). Finally, that for Fragilaria, the in situ loss processes are usually dominated by sedimentation of cells: colonies comprising more than 13 cells of > 60 ,tm in length are virtually immune from ingestion by filter-feeding zooplankton (Ferguson, Thompson and Reynolds, 1982).

The analysis is developed as follows: relevant observations are shown to broadly conform to a descriptive model based on two environmental variables - the depth of isothermal column mixing and the depth of light extinction; the same variables are used to predict maximal instantaneous growth rates, net of respirational losses, assuming both quantities to be direct correlatives of maximum photosynthetic rates; after subtraction of sinking loss rates, calculated from measured settling into in situ sediment traps, the modelled rates of population change are compared with actual observations. Finally, departures of the model predictions from the natural events are assessed in relation to qualitative observations on the condition of the cells made at the time.

MATERIALS AND METHODS

The observational data analysed here were mostly obtained during the period May to October, 1982; the methods and apparatus employed, the sampling procedures followed and the experimental observations have been described in detail in Reynolds, Wiseman and Clarke (1983a). Enclosure C (area, 1630 M2; mean depth, 9-9 m) was effectively isolated from the water of Blelham Tarn throughout the year. It was fertilized on several occasions with inorganic nutrients in quantities designed to obviate chronic nutrient limitation of phytoplankton growth; total areal loadings were equivalent to 23-6 gm-2 of soluble reactive silicon (SRS; = 50-6 g SiO2 m-2); 0-96 g m-2 soluble reactive phosphorus (SRP); and 11.1 g m-2 dissolved inorganic nitrogen (DIN). A purpose-built air-lift pump (see fig. 16 of Reynolds et al., 1983b), capable of raising hypolimnetic water at a rate of 200 m3 h- and discharging it at the surface, was operated periodically in order to rapidly depress the metalinmion and to then maintain an artificially-enlarged, mixed epilimnion (depth 8 m), for between 7 and 14 days at a time. During the intervening 1- to 3-week ('quiescent') periods, the enclosed water column was allowed to restratify, relying on heat transfer between adjacent levels across the enclosure wall. Apart from homogenizing the chemical composition and the vertical distribution of particulates through the upper 8 m, the imposed mixing also profoundly modified the light regime experienced by entrained phytoplankton, at once subjecting the organisms present to more extreme and more frequent oscillations in the perceived underwater irradiance and, often, effectively reducing the total perceived photoperiod.

The water was variously sampled, twice weekly. The data cited herein refer to vertical series of samples taken with the 1-m Friedinger bottle (Irish, 1980) at a fixed station (CD of Lund and Reynolds, 1982) near the deepest part of the enclosure; individual samples were bulked together to yield six collections,


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Production and dynamics of Fragilaria 43

respectively representing the layers 0 to 3, 3 to 5, 5 to 7, 7 to 9, 9 to 11 and 11 to ca. 13 m. The concentrations of Fragilaria cells were assessed by direct counts of sample aliquots, fixed on collection with Lugol's iodine and sedimented in the laboratory, following the inverted-microscope method (Lund, Kipling and Le Cren, 1958). Analyses of SRS in further aliquots of the same six samples were carried out weekly; a version of the colorimetric determination of reduced silico-molybdate (Mullin and Riley, 1955; Mackereth, Heron and Talling, 1978) was used.

Profiles of water temperatures were constructed for each sampling occasion from in situ measurements made with the resistance-thermometer circuit of a YS I Model 57 Oxygen Probe (Yellow Springs Instruments: Yellow Springs, Ohio). Light penetration was approximated from the recorded depths of disappearance of a white Secchi-disc, according to average relationships with direct photometric measurements, determined previously (George, 1983; Reynolds et al., 1983b).

A pair of cylindrical sediment-traps (see Reynolds et al., 1983b) were continuously deployed near station CD, 85 cm above the bottom in a depth of ca. 12 m. The traps were recovered fortnightly; aliquots of the well-mixed contents were sedimented and enumerated on the inverted microscope. Catches of Fragilaria were expressed areally (cells cm-2); the mean rate of settling into the traps was calculated as the vertical height of the column above the trap that would have to have been cleared of the (known) concentration of cells during the previous 14 days in order to have made up the observed catch (viz: cells cm-2/cells cm-3 x 14 x 100 = m day-'; cf. Reynolds and Wiseman, 1982).

Additional data on the growth rates of two Fragilaria strains in the laboratory were obtained by my colleague, Mr G. H. M. Jaworski. Cells were inoculated into the modified Chu medium of Lund, Jaworski and Butterwick (1975), enriched with soil extract, and growth for several days in temperature-controlled culture cabinets under continuous, saturating irradiances (> 227 ,tE m-2 s-1, PAR). Increase was followed in each of two replicates at each of three temperatures from spectro- photometric attenuance readings of the suspensions at 680 nm.

RESU LTS

Changes in the near-surface population of Fragilaria Seasonal variations in the abundance and vertical distribution of Fragilaria

are represented in the isopleth-diagram [Fig. 1(a)] and can be directly related to summaries of the sediment-trap recoveries [Fig. 1(b)] and of the variations in mixed depth (Zm, defined as the depth of water wherein the temperature gradient is uniformly < 1? m-1) and in the depth of Secchi-disc extinction (Zs), shown in Figure 1(c). These presentations confirm (i) that the phases of net increase and decrease are broadly correlated with changes in the mixed depth and (ii) that phases of decrease are accompanied by prolific sedimentation. Indeed, the variations in the standing concentration of Fragilaria cells in the upper 3 m of the enclosure (Fig. 2, N03) were observed to be particularly sensitive to the imposed changes in column stability and broadly conformed to the rates of net population change predicted by the modified descriptive equation of Reynolds et al. (1983b). This concurrence suggests that the assumptions of the model - that the net rates of change are influenced by the capacity of the mixed layer to entrain the population, long enough to divide and increase, but subject to its relative optical depth, and


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44 C. S. REYNOLDS

250

D 1 8 na)

?~~~1 6 (0)}t

12 125

4- di (a )

8 (D

1 0~~~2

4hw ././v0 Z VI} V

U) I~~~~~~~~~

-C ~ ~ ~ ~ 0

-0*853 12 1 I I

Jun Jul Aug Sep Jun Jul Aug Sep

Fig. 1. Fig. 2.

Fig. 1. (a) The vertical distribution of Fragilaria (isopleths in cells ml-') and (b) the mean daily rates of cell arrival into sediment traps (the data for both traps are shown on a log1o scale; the gap between the horizontal lines of each histogram is a measure of the disagreement between traps) in relation to (c) physical variables in Enclosure C (mixed depth, as the broader broken line, and Secchi-disc extinction depth as the narrower continuous line), influenced by episodes of artificial destratification (denoted by solid bands at the top of the Figure) or natural, weather-induced

column mixing (hatching).

Fig. 2. (a) Changes in the mean concentration of Fragilaria cells in the upper 3 m of Enclosure C and (b) a comparison of the rates of observed change between successive estimates (straight lines) and the daily rates of change predicted by the equation of Reynolds et al. (1983b):

knm = 0-292 loglo Zm - [1/{1 048- 0039(Zm/Z8)2}] +0-972.

that this effect is largely independent of limiting-nutrient constraints - are substantially applicable to the 1982 data. Moreover, it indicates that two opposing processes largely govern the dynamic responses of the population: photosynthetic productivity and sinking loss. Both are amenable to theoretical quantification.

Photosynthetic productivity Several steps must be taken in formulating the relationship between in situ

photosynthetic production and the rates of population increase. The first is to establish the capabilities of the photosynthetic system. Information in the literature on the light-saturated photosynthetic rates (Pmax) in laboratory exposures of


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Fragilaria suspensions is fragmentary, although there are sufficient data (Talling, 1957a, 1966; Harris and Piccinin, 1977; Reynolds, 1983) to suggest that the photosynthetic behaviour of Fragilaria neither differs greatly from that of Asterio- nella (for which extensive experimental data exist) nor, expressed per unit of chlorophyll a (chl a) pigment, from freshwater algae in general. I have deduced

from these sources a mean Pmax value of 10 5 ( ? 0 7) mg 02(mg chl a) h-' at 20 ?C

with a mean Qlo, between 5 and 20 ?C, of 2 19. If equimolar exchanges with carbon dioxide are assumed, the maximum carbon

fixation rate at 20 ?C is equivalent to 39( ? 0 3) mg carbon (mg chl a)-' h-'. From mean approximations of the chlorophyll (1D0 to 1P5 pg per cell) and the fraction (0 44 to 0 50) of the silica-free dry weight (150 to 200 pg per cell) of exponentially- growing F. crotonensis cultures (see Reynolds, 1983), a maximal rate of carbon assimilation into the cells may be proposed as

(3 9 + 0 3) (1P25 + 0-25)/(0A47 + 0-03) (175 + 25) = 0059(0 036 to 0 095) pg carbon (pg carbon)-' h-'

Correction must be allowed in respect of respirational and other carbon losses; typical values for the respiration rates (R) of diatoms fall in the range 0-02 to 0 11 PmaxX with the highest frequency between 0 04 and 0 07 (mean 0 055) Pmax (Talling, 1957a; Harris, 1978). This latter range is applied here. Probable net

photosynthetic production (Pmax-R) at 20 ?C may thus be taken as 0x056 (0 033 to 0 091) pg carbon (pg carbon)-' h-'. If devoted entirely to the assembly of new cell material (i.e. all other nutrient requirements are saturated), the assimilation of photosynthate would result in a 3 3 to 9 1 % increase in biomass for every hour that the assumptions continue to hold. Expressed as an exponential growth

constant (k' = ln (Bt/B0), where B0 expresses the initial biomass and Bt, that existing after 1 h):

k' = 0 054 (0 032 to 0 087) h-' 1 P302 (0-78 to 2 09) day-'

This result is directly comparable with the previously-reported estimates of maximum growth rate of Fragilaria in continuously light-saturated cultures at 20+ 1 ?C which are about 1P37 day-' (G. H. M. Jaworski, in Reynolds, 1983; see also below). It is clear that the observed rate of increase can be explained in terms of the theoretically-derived range of the maximum values sustainable by photosynthesis.

The effect of temperature The next step in the analysis was to show that the relationship between growth

and photosynthetic rates holds over a range of temperatures. Talling's (1955) data suggest this to be true for Asterionella, grown at temperatures between 4 and 20 ?C, and to be probably so for Fragilaria. Not only do they indicate a similar Qlo(= 2 3) for light-saturated growth but also that growth and photosynthetic rates are intraconvertible. Measurements of the growth rates of two strains of Fragilaria (L 331, 359) at three different temperatures, made in the present study, entirely support Talling's (1955) results: the slopes of the fitted curves, shown in Figure 3 correspond to Qlo values of 2-02 and 1P99. For the purposes of the present analysis


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46 C. S. REYNOLDS

1-6 /

7>. 1.2 -

0-8~~~

0-4~~~~

0.4 I l 5 10 15 20

0 (OC)

Fig. 3. The maximum rates of increase in two strains of Fragilaria crotonensis (@, L 331; 0, L 359) in continuously light-saturated cultures at three different temperatures.

it will be assumed that the growth of Fragilaria was limited only by net photosynthetic production, that the limitation of temperature upon growth rate

is identical with that upon Pmax; at a given temperature, 6, the growth rate will be given by:

k= k'20 (0.925)20-6 h-1.

The effect of underwater irradiance Besides the effects of temperature, it is necessary to accommodate the effects

of photoperiod and of the vertical light attenuation in Enclosure C on the photosynthetic production of Fragilaria. Gross photosynthetic rates of diatoms

generally become light-limited at irradiance intensities (Ik) in the range 50 to 120 jtE m-1 s-1 PAR (Harris, 1978). Following Talling's (1957c, 1971) recom- mendations, the integration of photosynthesis beneath a unit area of lake surface may

be approximated as the product of Pmax and ZO-5Ik (where ZO.5Ik is the depth at which the irradiance intensity is half the Ik value). Lacking frequent measurements of surface irradiance, of its extinction with depth or experimental determination of instantaneous Ik values, the present analysis suffers an immediate difficulty in approximating an average condition. Even assuming some constancy for the absolute value of Ik (which, given the acknowledged capacity of diatoms to adapt to low average light intensities, may not be an unreasonable assumption to make), its location will vary in depth during the course of the day and with changes from clouded to clear skies. The best approximation that might be made is to assume

that 0 5Ik (= 25 to 60 /aE m-2 s-1 PAR) represents between 2 and 25 % of the immediate sub-surface irradiance (I',) and, hence, that Zo.5Ik lies between 0 35 and 0 85 of the euphotic depth (Zeu). This range then embraces the point in the light gradient at which a Secchi-disc will generally 'disappear' when viewed from above the water surface (Zs 04 to 07 Zeu). For a given turbidity, the visible disappearance of a Secchi-disc is also sensitive to variations in insolation. Thus, to adopt the actual Secchi-disc measurements [Fig. 1(b)] as approximations of

contemporaneous depths, ZO.541k is not unreasonable. To do so, however, represents the weakest aspect of the development of the growth model.

A further constraint applies when the suspended population is actively mixed


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beyond the depth of saturating light intensities (i.e. Zm > Z,): cells are forced to spend part of the daylight period in water where photosynthetic production becomes markedly light-limited or is prevented altogether. The proportion that

is not so limited approximates to Z/Zm. At all times, photosynthetic production is confined to the daylight period (A).

Respiration, however, must be assumed to be continuous; therefore, estimates of growth rate (k') must be based on the daily integral of growth derived from the maximal hourly photosynthetic production potential at the temperature obtaining

(k'pq), corrected for day-length, sub-saturation and deep mixing; daily respirational loss rates are given as 24 x 0055k'pQ.

Growth-rate models The models that can be thus developed to predict instantaneous exponential

growth constants (k') of Fragilaria in the upper 3 m of Enclosure C and the conditions under which each applies are set out in Table 1. Four sets of eventualities are covered: model 1 applies when the depth of isothermal mixing lies within the upper 3 m and. is fully light saturated; model 2 applies when both

Zm and Z, lie within the upper 3 m; when the mixed depth extends beyond 3 m (such that the 0 to 3 m layer is integrated into a deeper-circulating layer but Zm

is still less than Z,) model 3 will apply (in reality, it is mathematically identical to model 1); in 'deep' mixed columns (Zm > 3 m and > Z,) model four will hold.

Table 1. Model equations generated to predict in situ growth rates of Fragilaria in the upper 3 m of Enclosure C and the environmental conditions under which each

applies

Model No. Condition Model equation

1 Zm < 3 m; Z8 > 3 m k' = Ak'po-24x OO55k'po 2 Zm < 3 m; Z8 < 3 m k' = Ak'po Z8/3-24x OO55k'po 3 Zm > 3 m; Z8 > Zm k' = Ak'po Zm/Zm-24 x O0055k'po 4 Zm > 3 m; Z8 < Zm k' = Ak'po Z8/Z8-24 x O0O55k'po

Interpolating values of day-length (sunrise to sunset, to the nearest 0.1 h) and

field measurements of Zm, Z, and of mean temperature in the upper 3 m, and putting k'p = 0,057 h-1 at 20 ?C (i.e. without correction for respirational carbon losses), the appropriate models have been solved for selected dates during the period June to September (inclusive). The results are shown in Figure 4. The resultant curve must be regarded as showing the fluctuation of the mean maximum level of the instantaneous growth rate that can be proposed and need not be representative of the growth rates that were actually achieved. Nevertheless, the plot reaffirms clearly that growth rate is likely to be highly sensitive to variations in the physical characteristics of the enclosed water column.

In situ sinking losses The dynamics of net population changes among planktonic diatoms are

influenced by instantaneous rates of loss as well as by growth, even among healthy, actively-growingpopulations (see, for instance, Knoechel and Kalff, 1978; Reynolds and Wiseman, 1982). Being non-motile and having a relatively high density (-& 1200 kg m-3; Reynolds, 1983), Fragilaria colonies have relatively high sinking


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48 C. S. REYNOLDS

1*2

0.8 -

0 4-

0-0'

-0-8

-1-2-

Jun Jul Aug Sep

Fig. 4. Solutions to the photosynthetically-derived growth rates, k' (open circles), the ranges of the instantaneous sinking loss rates, k8 (pairs of open triangles), and the calculated range of the net rate of population change knm = k'-k8 (the vertically hatched band), compared with the observed rate of change, knm (from Fig. 2) and the changes in column stability (represented at the

top of the figure, as in Fig. 1).

-o 1 0 + +

H0-5 -

I | l ~ ~ ~ ~~~~~~~~~~ I I Jun Jul Aug Sep Oct

Fig. 5. The ranges and means of sinking rate (VT) approximated from recoveries of Fragilaria cells in the sediment traps through each trapping period.

velocities (v'). Various approximations of v' are available for Fragilaria (01 to 0-6 m day-1; see Reynolds, 1983): they are known to vary with temperature, chain length and, most importantly, with physiological condition (three to sevenfold variations between healthy and dead colonies have been noted). Suspension is dependent upon the entrainment within turbulent eddies to delay settling of populations from mixed layers but colonies are readily disentrained from laminar flow or from low current velocities in the vicinity of the metalimnion (Walsby and Reynolds, 1980). The instantaneous exponential rate of sinking loss (k8) from fully-developed turbulent columns, of depth Zm, into non-turbulent water below is directly proportional to -v'/Zm (Smith, 1982).


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Sinking velocity was not separately measured in the present study. However, estimates of the mean rate of settling into sediment traps (VT) were calculated for each 14-day trapping period (see Fig. 5). It cannot be assumed of course that VT is simultaneously identical with v' near the surface although the former is scarcely likely to consistently underestimate the latter. Moreover, as Figure 5 shows, VT was itself a sharply variable quantity. Between late May and early July, VT was estimated to be between 0 12 and 023 m day-' and it remained <0-4 m day-' through much of the summer (i.e. well within the range observed among healthy cells). The sharp increases in VT, observed in late June, early August, early September and early October are therefore of special interest. It was noted at the time that the Fragilaria catches were dominated by live cells having the contracted protoplasts and shrunken plastids symptomatic of cells exposed to inhibiting near-surface light intensities (cf. Harris, 1978). If the high sinking rates are genuine and attributable to conditions obtaining in surface waters, then it is possible to determine the approximate dates when such episodes of accelerated sinking commenced, as set out in Table 2. In each instance, the span of back-calculated dates coincides well with a period of observed net depletion of the Fragilaria population in the upper 3 m (shown in Figs 2 and 4) which, in turn, coincided with an abrupt diminution of the mixed depth in response to intense insolation and near-surface microstratification. These evident correlations suggest that the substitution of upper and lower limits of VT for v' to solve k8 for the corresponding occasions, as represented in Figure 4, is not unrealistic. By analogy, VT evaluations outside the trapping periods listed in Table 2 may be applied to approximate the likely range of in situ sinking rates at other times (mean, 0288 m day-1; s.e. + 0107 m day-1): the upper and lower limits of the error (0181,

0395 m day-1) are used to estimate the range of k. for the remaining occasions represented in Figure 4.

Table 2. The periods of rapid settling rates of Fragilaria colonies into sediment traps and back calculations of the periods in which accelerated sinking losses may have

occurred

Time to sink Period when Period vT(m day-') 12 m (days) sinking commenced

22 June to 6 July 0 539 to 0 563 21 3 to 22-3 31 May to 15 June 3 Aug. to 18 Aug. 0-629 to 0-637 18-8 to 19-1 17 July to 31 July

31 Aug. to 14 Sep. 0 773 to 1 063 11 3 to 15-6 15 Aug. to 3 Sep. 28 Sep. to 12 Oct. 0 616 to 0 783 15-3 to 19-5 9 Sep. to 23 Sep.

Prediction of the rates of net change

The final step in the analysis is to deduct the calculated range of k. from the possible photosynthesis-determined k' values to yield the predicted range of net population change (ku). The resultant fluctuations in the range of kn are traced in Figure 4, where they may be directly compared with the observed exponential rates of change. The most striking feature of the comparison is the often-large discrepancy between the predictions and the observations. Generally, the former exceed the latter and their trend, especially, is the opposite of what was actually detected. In contrast, the actual rates of change during mid-June, late July, mid- to late-August and early September (periods in which the water column was


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50 C. S. REYNOLDS

well-mixed to depths of 6 to 8 m) are reasonably well predicted by the model solutions. The exaggeration here varies by as little as 002 day-' during August and September and < 008 day-' in June and July. The model also underestimates the apparent surges of growth detected at the starts of these periods when, presumably, the net rates of change were influenced by the inoculation into the surface circulation of colonies air-lifted from the hypolimnetic depths to which they had sedimented after earlier maxima; this eventuality is not covered by the model. Accepting these limitations, the observed rates of increase during periods of mixing are well-predicted by the model solutions. This would indicate that Fragilaria was then growing close to its theoretical photosynthesis-limited capacity.

Equally, the proposed photosynthetic capability of Fragilaria was not translated into commensurate growth rates during the quiescent periods, when the water column stabilized to within 2 or 3 m of the surface. Indeed, the actual rates of

population decline are more closely approximated by the values of k. alone (i.e. kn -k5). The inference must be that, far from maintaining the theoretical maximum rate of growth, Fragilaria virtually stopped growing altogether, while the coupling of reduced mixed depth and an accelerated rate of sinking contributed to its rapid elimination. Indeed, sinking rates of between 05 and 1 1 m day-' scarcely characterize healthy, actively-growing Fragilaria populations (see Reynolds, 1983). Further evidence of a poor growth response of diatoms to column stability may be drawn from contemporaneous changes in the areal concentration of soluble reactive silicon: the June, July and August periods of Fragilaria growth are, as expected, matched by hyperbolic declines in SRS content (Fig. 6) but the curves flatten out when Fragilaria was in rapid net decline (as in the quiescent phases).

E t; ~ ~ ~~~~~~~~~~~~~~~~I I *--- I@- Jun Jul Aug Sep

Fig. 6. The areal concentration of SRS (as mg SiO2 cm-2) in Enclosure C during 1982; the abrupt increases correspond with additions of inorganic sodium metasilicate.

The combined evidence of low growth, high sinking and sinking loss rates and of cytological disruption points to severe photoinhibition of Fragilaria cells 'stranded' within the upper euphotic layers during extreme column microstratification. Photoinhibition of photosynthetic production is known to occur at irradiance levels in excess of 300 to 600 tE m-2 s-1 PAR (see plot of values, quoted from the literature, in Harris, 1978); the extent of the effect is influenced by the intensity, quality and duration of near-surface underwater irradiance and by the recent light-histories of the photosynthetic organisms. Erstwhile deep-mixed populations of diatoms are particularly prone to rapid photoinhibition and declining photosynthetic efficiency after a few minutes' exposure to irradiance equivalent to full sunlight (Harris, 1973; Harris and Piccinin, 1977). Moreover, recovery from photoinhibition, involving replacement of damaged photosystems, can take several days. The only immediate escape is offered by enhanced sinking


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Production and dynamics of Fragilaria 5I

rates. It therefore seems likely that, in the present instance, Fragilaria cells that had maintained a relatively high photosynthetic efficiency and sustained high photosynthetically-regulated rates of growth whilst freely circulating through well-mixed columns became subjected to intolerable levels of solar radiation in the upper part of the column when the mixing weakened and they were neither able to readapt before settling into deep water nor to recover their epilimnetic position until the next phase of artificial mixing. Active mixing through the water column, however, ensured that exposure to high irradiances were correspondingly brief, photoinhibition was negligible and that high photosynthetic efficiencies and maximal theoretical growth rates could be maintained.

DISCUSSION

The foregoing analysis amply supports previous statements (Talling, 1955; Lund, 1964; Harris, 1978; Reynolds, 1983) that there is frequently a good correlation between growth and photosynthetic behaviour among non-nutrient limited populations of diatoms. This implies the existence of mechanisms for ensuring efficient and rapid assimilation of photosynthetically-fixed carbon with relatively small metabolic loss. The conditions which are favourable for photosynthetic production of diatoms are presumably the same as for other planktonic photoautotrophs but the means of regulating photosynthesis and the conditions ideal for efficient population growth differ among the phytoplankton. For example, the diatoms are overtly dependent upon deep-mixing of the water to overcome heavy sinking losses; this inevitably means that populations will be exposed to high-frequency fluctuations in irradiance which, in extreme, ranges from full-light to effective darkness. The photosynthetic behaviour of diatoms is evidently well-tailored to such conditions: in particular, the photoadaptive responses enable photosynthetic efficiency to be enhanced at low average irradiance levels and facilitate rapid photosynthesis in short exposures to high ones. Although the excretion of photosynthetic intermediates (e.g. glycollate) provides one mechanism of regula- tion, these adaptations carry the penalty that, if the mixing is abruptly reduced, cells are liable to severe photoinhibition and damage to the photosynthetic apparatus. Whereas planktonic representatives of other algal groups can deal with these problems by invoking photorespiratory mechanisms or, commonly, by self-regulated surface-avoidance movements, diatoms apparently have no defence other than to accelerate their sinking into deep water. Even if the photoinhibition is temporary and physiological recovery is rapid, the continuing weakness of turbulent diffusivity denies them either a quick positional recovery or the opportunity to increase their numbers.

These elements are incorporated in the modified descriptive model of Fragilaria dynamics (Reynolds et al., 1983b), which, as the current data show, predicts net changes with reasonable accuracy. Without suggesting their precise roles, the model does relate empirically to the absolute and optical depth characteristics of the mixed column. The latter must be able to support net photosynthetic production and to be deep enough to ensure that productive gains exceed sinking losses. This requirement is of at least equal importance to the nutrient requirements of diatoms. Indeed, it is frequently the critical factor influencing net increase or decrease of populations, even when the nutrient requirements are saturated (Reynolds, 1973; Reynolds and Butterwick, 1979). It is not entirely speculative to suggest that the seasonal abundance of diatoms in temperate lakes, during the


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52 C. S. REYNOLDS

spring and autumn and in short summer bursts, is dependent upon the more deeply-mixed, physically-variable water columns obtaining at such times, so long as nutrients are available to support growth. The evidence from the intermittently- mixed water column of Lund Tube C strongly supports this contention.

ACKNOWLEDGEMENTS

I wish to -thank Sheila Wiseman, Mike Clarke and Sarah Gatehouse for their capable assistance in obtaining the data upon which the present analysis is founded. Special thanks go to G. H. M. Jaworski who carried out the growth rate measurements on laboratory cultures of Fragilaria. I am also grateful to Dr John Hilton and his colleagues, for the chemical analyses quoted herein, to Brian Godfrey and Peter Allen for maintaining the Blelham Enclosures and the air-lift apparatus, to the National Trust who gave permission for the work to be carried out in Blelham Tarn and the Department of the Environment and the Natural Environment Research Council who jointly funded the work (Contract DGR/41 0/380).

REFERENCES

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