temporal variability of zooplankton biomass (atp content and dry weight) in the st. lawrence...

Marine Biology 73, 247-255 (1983) Marine . . . . . . . . . . . . . . . . . . Biology

�9 Springer-Vedag 1983

Temporal Variability of Zooplankton Biomass (ATP Content and Dry Weight) in the St. Lawrence Estuary: Advective Phenomena During Neap Tide *

Y. Maranda ** and G. Lacroix

GIROQ, D6partement de Biologie, Universit6 Laval; Qu6bec, Canada

Abstract

In order to assess the temporal variability of living zooplankton in a tidal estuary, the ATP content and dry weight of mixed zooplankton populations (mainly copepods) were measured during a period of 175 h at an anchor station in the Upper St. Lawrence Estuary. Vertical tows were made every 30 rain. Hourly vertical profiles of the current speed and direction, temperature and salinity were also obtained during the experiment. A strong tidal influence was found in all series. Maxima and minima of the ATP ~ontent (living biomass) and the dry weight (total biomass) were correlated with low and high water slacks. The serial autocorrelation and cross-correlation showed, in both series a 12 to 13-h cycle, and the ATP:dry weight ratio showed a significant 24-h cycle. The cross-correlation with the Kendall r was used to detect the relationship between biological components and physical indices (stratification and Ri). It is suggested that the proportion of living zooplankton biomass in the Upper St. Lawrence Estuary is most likely the result of a combina- tion of diurnal migration and longitudinal advection.

Introduction

Estuaries are dynamic environments where advective and mixing processes may create a stressing habitat for living organisms, particularly for the zooplankton which are dependent on water movements. Distributions of zooplankton would not only be determined by factors such as swimming activity, life cycle and geographical patterns of reproduction, but also by physical processes (Rogers, 1940;

* Contribution to GIROQ program (Groupe interuniversitaire de recherches oc~anographiques du Quebec)

** Present address: D~partement des sciences fondamentales, Universit~ du Qudbec /t Chicoutimi; Chicoutimi, Quebec G7H 2B 1, Canada

Ketchum, 1954; Barlow, 1955; Bousfield, 1955; Riley, 1964; Jacobs, 1968; Wood and Hargis, 1971).

Periodic fluctuations of the zooplankton biomass and species composition were previously found to be correlated with the tide (Sameoto, 1975~ 1978; Gagnon and Lacroix, 1981). For example, in the latter paper, the authors studied the effects of tidal advection and mixing on the statistical dispersion of zooplankton dry weight and developed an interpretative model of the sampling variability in the Upper St. Lawrence Estuary. However, in no other studies were the short-term fluctuations of living zooplankton reported. The biomass of living zooplankton was measured by the usual extraction procedures, which were reported to be a good index of living biomass (Holm- Hansen and Booth, 1966; Hamilton and Hohn-Hansen, 1967; Traganza and Graham, 1977; Skjoldal and Bam- stedt, 1977; Karl et al., 1978).

This paper examines the estuarine temporal variability of living zooplankton and attempts to relate it to the mixing conditions using physical indices of stratification and stability over a period of 175 h at a fixed station in the Upper St. Lawrence Estuary. This estuary is considered a partially mixed system where semidiurnal tides are of large amplitudes (4 m) with steep salinity and temperature gradients (Bousfield et al., 1975).

Materials and Methods

Sampling Procedures

The sampling program was carried out at an anchor station in the lower part of the Upper St. Lawrence Estuary (Fig. 1). Vertical tows of zooplankton were made from the bottom (30 m) to the surface, using a 50-cm :~ 10 standard mesh net (158 #m) equipped with a flow-meter. The zooplankton was collected every 30 min during 7 d in August (2-9) 1976 for a total of 349 samples.

248 Y. Maranda and G. Lacroix: Temporal Variability of Zooplankton Biomass

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Two subsamples were obtained from each sample with a Nival splitter (Nival and Nival, 1973). Large organisms (euphausiids, mysids, chaetognaths) were removed from the samples before splitting to ensure comparable subsamples for the biomass determinations (ATP content and dry weight). One subsample (in 4% formaldehyde) was used for dry weight measurements (Beers, 1976) and for identification, and the other for ATP extraction (Holm- Hansen and Booth, 1966; Daumas, 1973; and Bamstedt and Skjoldal, 1976). Considering the mean number of individuals (100-150) in the subsample, ATP extraction was done on an aliquot of this subsample. A fixed representative volume (4 ml) of the subsample was poured into 40 ml of boiling Tris buffer (pH = 7.78; 0.02 M; Sigma Chemical Co.) in order to perform a good extraction (Maranda, 1981) before freezing the aliquot a t - 2 0 ~ ATP was determined with a photometer (SAI Technology Co., model 3000) using the luciferin-luciferase light reac- tion of firefly extract.

Vertical distribution of temperature, salinity and current velocity were obtained from hourly records taken at seven depths (1, 5, 10, 15, 20, 25, 30m) with an Aanderaa current meter.

Data Processing

Biomass data were converted to units of biomass per cubic meter and transformed to log10 (x+ 1) in order to normal- ize the distribution and to decorrelate the mean and variance of the data. The ATP:dry weight series were normalized by the V x+ 1 transformation. The Pearson

correlation coefficient (r) was calculated when the distribution of the variables was not found significantly different from the normal distribution (P < 0.05), using the Kolmogorov-Smirnov test. Otherwise, the Kendall non- parametric rank correlation coefficient (~) was used.

A stationary series was obtained from the normalized data; linear and/or parabolic trends were removed by fitting a polynomial expression using the least square method (Legendre and Legendre, 1979). We also used low pass filters to separate high and low frequencies of the transformed series. The tidal variability (M2) was ex- tracted using a shaped moving average of 26 values for a sampling interval of 30min, and of 15 values for a sampling interval of one hour. Residual series were obtained by substracting the filtered series from the raw series.

Serial autocorrelations and cross-correlations (Cox and Lewis, 1966) were applied to the unfiltered and filtered series and to the high frequency fluctuations in order to extract the periodicity and to detect the relations between pairs of variables. The Kendall T was calculated with the cross-correlation when the distribution differed from the normal law (P < 0.05).

Results

Short-term Physical Variability

In the Upper St. Lawrence Estuary, the semidiurnal tides are about 4 m in amplitude. Sampling took place mainly during neap tides. Plots of the progressive vector diagrams

Y. Maranda and G. Lacroix: Temporal Variability of Zooplankton Biomass 249

show a net downstream outflow at each depth, but sometimes a typical two-layer flow circulation is revealed (Fig. 2). Gagnon and Lacroix (1981) observed the same pattern during neap tides about 30 km upstream. It is also evident from these diagrams that the back-and-forth circulation of the tide is stronger in the deeper layer. The surface water continually flows downstream but slows down when the tide is coming up in the deeper layer.

Vertical mean at gradients between one and 30 m were used as stratification indices. The quadrature-neap tide period is revealed by such gradients (Fig. 3 A). The autocorrelation of the at series suggests a 12 to 13-h cycle, matching the period of the tide (Fig. 3 B). Series filtration does not add much information except the existence of some variability at high frequencies. The analysis of other at vertical gradients from shallower depths shows a similar pattern even though the tidal influence is lessened near the surface layer.

To characterize the vertical stability, the Richardson number (t~i) was calculated (Fortier and Legendre, 1979). The absolute values of Ri, as computed here, actually have a restricted significance from a physical point of view; nevertheless, they probably give a reliable index of the relative stability of the water column on a time basis. The hourly variation of l~i reveals a cycle consisting of periods of strong stability (high Ri) and periods of potential vertical mixing (low Ri) (Fig. 3 C). The autocorrelation of the series confirms a 12 to 13-h cycle (Fig. 3 D), as for the at gradients. The cross-correlation between at and l~i series shows a significant negative

correlation, the l~i series lags by 1 to 2 h behind the at (Fig. 4). This lag suggests that at and Ri do not express the same properties of the water column.

Short-term Zooplankton Variability

The zooplankton species are composed mainly of copepods (more than 85% of the species), of which 50-70% are Acartia spp., mainly A. longiremis. The other taxonomic units are in order of decreasing importance: Euryfemora sp., copepod nauplii, cypris larvae, Oithona similis, Cala- nus finmarchicus and occasionaly small mysids, poly- chaetes and gastropod larvae.

The raw data series of the biomass indices (ATP content and dry weight) show periodic amplitude variations which correspond approximately to the one of the tide (Fig. 5A, 5B). Minima and maxima are generally associated with high water and low water slacks, respectively. A change in the fluctuation pattern and a loss of regularity are observed during neap tide between the 60th and the 90th hour. The amplitude variations of the dry weight data are greater after the 90th hour than during the first 60 h. A linear trend can be seen from the 175-h series; unfortunately because of the shortness of the series, it cannot be ascertained whether the trend is a part of a fortnightly cycle.

The three maxima observed at the beginning of the series of ATP content (Fig. 5 A) most likely result from the presence of a swarm of young mysids included in the

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samples. As a result of time constraint in the extraction procedure, it was impossible to remove these organisms completely.

Fig. 5 C shows the fluctuations of the ratio of the ATP content (living biomass) to dry weight (total biomass) with time. Values of both series have been gauged through the maximum of its series (y '= y /y max.) yielding new sets of dimentionless data of comparable magnitude (Cain and Harrison, 1958). Temporal fluctuations of these ratios have an oscillation pattern different from the ATP and dry weight series. The semidiurnal cycle of the ratios is partially hidden by a 24-h cycle.

By filtering the data, the ATP content and dry weight series are shown to be out of phase by about 180 ~ with the

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tidal oscillation (Fig. 6A, 6B). A 12-h and a 24-h cycle may be detected from the filtered ratio series (Fig. 6C), although the 24-h cycle is more evident during some 64 h after the 60th hour. The residual series (Fig. 6 D, 6 E, 6 F) of ATP, dry weight and the ratio represent the variability at high frequencies. The autocorrelograms of the log- transformed data and the filtered series of the ATP content (Fig. 7A, 7D) and the dry weight (Fig. 7 B, 7E) significantly point out a 12 to 13-h cycle, whi lethe residual series (Fig. 7F, 7G) indicate a 6-h cycle. The autocorrelogram of the whole transformed ( V x + 1) ratio series indicates a significant diurnal cycle (Fig. 7 C).

Relationship Between ATP, Dry Weight and the Physical Parameters

A very significant correlation (P<0.01) between ATP content and dry weight is found in the log-transformed series (r=0.594; n=349) , in the filtered series (r=0.770; n = 299) and in the residual series (r = 0.433; n = 299).

Since the biomass was estimated twice per hour and the physical value only once, removal of every other biomass value in the whole series was necessary to correlate the biomass data with the physical parameters. The serial cross-correlation (Kendall r) confirms that the raw series


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of biomass data (ATP content and dry weight) are approximately in phase with mixing conditions (Ri) in a 12-h cycle (Fig. 8A, 8B). In both cases, the correlation is negative and significant (P < 0.05). The correlation is significant for a lag of 2 - 3 h between biomass and ot gradients (Fig. 8 D, 8 E). Although cross-correlations show similarities between the ATP:dry weight ratios, the Aat and the l~i series, values of these parameters are not significantly correlated (Fig. 8 C, 8 F).

Discussion

This work focussed on the assessment of the temporal variability of zooplankton. Some insight into the processes involved in the survival of zooplankton organisms may be obtained from the correlations of zooplankton living biomass (ATP content) with the total biomass (dry weight) and from the following assumptions:

(1) ATP content is a valid estimate of living matter (Holm-Hansen and Booth, 1966; Daumas, 1973; Bamstedt and Skjoldal, 1976; Skjoldal and Bamstedt, 1977; Tra- ganza and Graham, 1977; Karl et al., 1978).

(2) Measurements of the ATP content made on multi- species zooplankton samples are reasonably devoid of gross errors. ATP extraction from the zooplankton with boiling Tris buffer underestimates the total ATP content (Karl et al., 1978). Nevertheless, insofar as the aim is to evaluate trends, the ATP values presented here are pro- portional to the ATP content of the sampled population. Moreover, the major trends and correlations found in a fluctuating environment, such as the St. Lawrence Estuary, are not altered by the size of this underestimation. ATP:C ratios, which are less appropriate when a mixed zooplankton is bound by large environmental fluctuations and when physiological rythms are involved, were not used for this reason (Bamstedt and Skjoldal, 1976; Skjoldal and Bamstedt, 1977).

(3) Large differences between the ATP and the dry weight series would be mainly due to change in the species composition or to in-sizu mortality related to rapid mixing of advected zooplankton structures (Weikert, 1977), however, estuarine copepods are somewhat insensitive to the latter effect (Lance, 1963; Riley, 1964). In both cases, differences between the ATP content and the dry weight


series would have a tidal component and should be associated with some indices of vertical stability.

The zooplankton series may be seen as oscillations of short and long wavelengths and the main period involved is about 12 h. The change in the amplitude of the ATP content and the dry weight series between the 60th and the 90th hour would have resulted from the multiplication of a wavelength by another one of lower frequency (e.g. 12-h cycle with a fortnightly cycle). The 6-h cycle found in the autocorrelograms (Fig. 7A, 7B) may be the result of the tag between the surface layer, which flows downstream, and the bottom layer which flows back-and-forth with the tide, since both living biomass (ATP content) and total biomass (dry weight) series have the 6-h as well as the 12-h period. These tidal components are the main vectors in temporal fluctuations of zooplankton at the anchor station.

On the other hand, the ATP:dry weight ratios show a prevalent 12-h cycle during the first 60 h (quadrature), and a prevalent 24-h cycle for the next 64 h (neap tide). Higher values in both segments of the series are associated with the falling tide, mainly with night periods, and with strong potential mixing (l~i) at the anchor station.

The lag of 2-3 h between the minimum stratification (Aat) and the maximum of the ATP content and the dry weight is explained by the lag between the surface layer, which flows continually downstream (Fig. 2), and the bottom layer, which is coming up at flood tide 2-3 h after the low water slack. As the core of the density gradient is presumably located between these two water masses and oscillates with the tide, the vertical current shear might combine with the vertical migration to produce zooplankton patches as suggested by the model of Evans et al. (1977) for non-tidal waters. But the stratification, estimated here as the difference in at between 1 and 30 m, could be a mere result of mixing conditions on the whole water column at the anchor station.

The relationship between relative increments in the proportion of living zooplankton (ATP:dry weight ratios) with the ebb tide, darkness and the poor stratification suggests an advection from upstream of zooplankton previously influenced by diurnal migrations. Deep populations of zooplankton from the upstream basins (more than 75 m deep), including large marine species like Calanus

finmarchicus and C. hyperboreus, would swim up for feed- ing in.the middle layers during the night (Bousfield et aI., 1975) and then could be advected downstream at ebb tide over the shallower areas (e.g. the anchor station). As long as the advected populations are not physiologically dam- aged in the low salinity surface layer, they would have a higher proportion of the living matter than would the populations of small brackish-water species rapidly advected from the low salinity upstream waters to high salinity downstream waters. At ebb tide and in daylight, the downstream advection of zooplankton could not in- clude these deep forms and the resulting sampling would produce the lower biomass and the lower relative values of ATP observed at the anchor station.

Thus, there is evidence that periodical variations in the mixing conditions, the stratification and the differences in the vertical profile of the water circulation are involved, presumably as modulators of the amplitude of the zooplankton variability (Gagnon and Lacroix, 1981) and likewise of the living zooplankton variability, in the problem of the survival of zooplankton populations in an estuary.

Acknowledgements. This work was supported by funds from the National Research Council of Canada and by the Quebec Department of Education to GIROQ (Groupe interuniversitaire de recherches ocdanographiques du Qu6bec). Special thanks are due to Drs C. L. Trump, L. Legendre, R. C6t6 for their helpful criticisms, Dr. Y. Ouellet for the use of his computer facilities and M. Y. Roy for his good work on the computer.

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Date of final manuscript acceptance: January 24, 1983. Communicated by R. O. Fournier

temporal variability of zooplankton biomass (atp content and dry weight) in the st. lawrence...

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