Seasonal variation in abundance and size structure of phytoplankton in Baiedes Chaleurs, southwestern Gulf of St . Lawrence, in relation to physicaloceanographic conditions
Michel R. Claereboudt, Jean Cote, John C . Bonardelli & John H . HimmelmanDepartement de biologie and GIROQ (Groupe interuniversitaire de recherches oceanographiques du Quebec),Universite Laval, Quebec, GI K 7P4 Canada
Received 16 December 1993 ; in revised form 24 May 1994 ; accepted 8 June 1994
We investigated changes in the abundance and size structure of phytoplankton and organic seston in relation totemperature, stratification and current patterns at Gascons on the north shore of Baie des Chaleurs, eastern Canada .Phytoplankton biomass showed a general decrease during the study (May to November 1989), except for a briefdiatom bloom in late October. During most of the summer, a strong temperature driven stratification was present and<5 µm cells dominated the phytoplankton community. Particles measuring <5 µm also dominated the particulateorganic matter (POC and PON) throughout the year . However, only 40% of these particles could be associatedwith phytoplankton cells . For both particulate matter and phytoplankton, the abundance of the <5 ttm size fractionwas positively correlated with the Brunt-Vailsala index of stability of the water column . Inorganic nitrogen mayhave limited the phytoplankton growth, as generally reported for stratified environments . Most of the biomass wasprobably supported by nitrogen regenerated through microbial organisms . A large bacterioplankton communitywas suggested by the abundance of small (<5 µm) non-phytoplanktonic particles with a low and relatively uniformC/N ratio. Larger particles were only abundant at the beginning of the study (May-June) and on one date in October .Their C/N ratios indicated they were of varied origins .
147
Introduction
The structure of phytoplankton communities is deter-mined by the equilibrium between production, expor-tation and grazing, and major driving forces are hydro-dynamic processes . According to Legendre & LeFevre (1991) the strong hydrodynamic events, riv-er inputs and anthropogenic eutrophication in coastalzones lead to highly productive ecosystems dominatedby large phytoplankton cells, whereas stable ocean-ic systems are oligotrophic and dominated by small(<5 µm), picoplanktonic cells . Recent studies havedemonstrated a much greater importance of picoplank-ton than originally thought and thus markedly changedour understanding of pelagic ecosystems (Stockner &Antia, 1986 ; Stockner, 1988) . Several reports showthat picoplankton are ubiquitous and in a wide vari-ety of environments may account for a large part of
primary production (Bienfang & Takahashi, 1983 ;Smith et al ., 1985). Nevertheless, the importanceof picoplankton in temperate coastal systems is notwell documented, particularly in relation to seasonalchanges in oceanographic conditions .
Early studies in Baie des Chaleurs, the largest bayin the Gulf of St. Lawrence, were done between 1938and 1967 by biologists at the Station de biologic marinede Grande-Riviere (Boudreault, 1968) . Recent stud-ies by Bonardelli et al . (1993) and LeQuere (1992)support, in part, suggestions by Tremblay (1944) andLegendre & Watt (1970) of a westward flow alongthe northern shore (Quebec) of the bay and an east-ward flow along the southern shore (New Brunswick) .These most recent studies also demonstrate the impor-tance of low-frequency variability in temperature andcurrent velocity, correlated with wind events whichperiodically cause upwelling . The annual development
148
of the zooplanktonic community in the bay is stronglyrelated to temperature conditions (Lacroix & Filteau,1969). The only studies providing information on thephytoplankton community in Baie des Chaleurs areBrunel's (1962) report of the taxonomy of large phy-toplanktonic species and observations by Legendre &Watt (1970) and Legendre (1973) on phytoplanktonbiomass, production and spatial distribution on severaldates in 1956, 1968 and 1969 .
The present study investigates seasonal changes inthe abundance of pico- (<5 pm), nano- (5-20 pm) andultra- (>20 jam) phytoplankton and organic particulatematter in the Baie des Chaleurs . We focus on the rela-tionship between seasonal changes in phytoplanktonabundance and size structure, and physical conditions,temperature and stratification . This is the first report ofthe seasonal development of the phytoplankton com-munity in Baie des Chaleurs .
Methods
The sampling for our study was made from May toDecember 1989 at Gascons (48 '10'55" N, 64 °54'58"W), on the north shore of the Baie des Chaleurs (Fig . 1) .The depth at the sampling site was 25 m and the bottomconsisted of cobbles and gravel .
We collected water samples at 3, 5, 9, 15, 21 and24 m using 8 1 Niskin bottles each Monday morningbetween 9 :00 and 11 :00 am . The samples were trans-ported to the laboratory in insulated opaque plastic con-tainers. They were passed through filters to separatethe suspended particles into different size fractions .Macroplankton was initially removed using 153 jammesh Nytex screens and then the samples were divid-ed into 11 aliquots . The aliquots were pre-filtered usingeither a 20 pm Nytex screen or a 5 pm Nucleopore filterand were then filtered onto pre-combusted WhatmanGF/F fiberglass filters . Three size classes, 0.7-153 pm,0.7-20 pm and 0 .7-5 pm, were thus obtained on thefilters . For each fraction, we made two determinationsof the chlorophyll a content using a Turner fluorime-ter (model III) following the procedures described byStrickland & Parsons (1972) . Two other filters werefrozen at - 20 °C for later determinations of partic-ulate organic carbon (POC) and particulate organicnitrogen (PON) using a Perkin Elmer CHN analyzer(model 240). Chlorophyll a measurements were madefor all six depths whereas POC and PON analyses wereonly made for 9, 15 and 21 m . We calculated chloro-phyll a, POC and PON concentrations for particles in
three size ranges, 0 .7-5 pm, 5-20 pm and 20-153 pmfrom the differences in the determinations for the var-ious filters.
On the same sampling dates, we further measuredwater transparency using a Secchi disk . The extinctioncoefficient was calculated using the formula for coastalwater (Holmes, 1970) and the depth of the euphoticzone (I% irradiance) was then estimated .
Current speed and direction, water temperature andconductivity were recorded at 30 min intervals at 9,15 and 21 m in depth using Anderra RCM-4 currentmeters. SCUBA divers regularly cleaned the currentmeters with brushes to prevent excessive fouling devel-opment. Additional continuous temperature recordswere obtained at 3, 5, 7, 9, 15 and 21 m in depthusing Ryan thermographs and were used to examinevariations of isotherms across the water column dur-ing the study .
Water density (sigma-t) was computed at 9, 15,and 21 m from the current-meter temperature and con-ductivity measurements . Then the stability of the watercolumn was determined using the Brunt-Vi ilsala staticindex (N), which was calculated as follows :
N2 - g (Px+1 - M1036X
'
where (p = density * 103 ; g = gravity ; SX = difference indepth (m) .
Results
Phytoplankton biomassSince temporal variations in chlorophyll a concentra-tion were significantly correlated at the five depthssampled, we calculated a depth-integrated chloro-phyll a concentration (mg m -2) for each samplingdate. Over time this value showed an alternating pat-tern of increases and decreases, possibly resulting fromthe superimposition (aliasing) of the tidal cycle on ourweekly sampling interval (Fig . 2A). In addition, it indi-cated a general decrease from spring to fall, exceptfor a single sample on 28 October (Fig . 2A) . In thespring, the chlorophyll a concentration was high andmore or less equally distributed among the three sizefractions examined (Fig . 3A) . In contrast, during thesummer and autumn, picoplankton (<5 am) account-ed for >70% of the chlorophyll a in the water column(Fig. 3B) . The increase in relative abundance of smallcells in early July was abrupt, and coincided with adrop in the abundance of larger cells . In contrast, the
decrease in small cells in the fall was more progres-sive (Fig. 3A). The exceptionally high level of chloro-phyll a on 28 October 1989 was due to cells measuring5 to 20 pm (Fig . 3A). More than 90% of these wereSkeletonema costatum and Leptocylindricus danicusand these diatoms were almost absent on other datesduring our study (B . Hupperts, DFO Canada, Insti-tut Maurice Lamontagne, personal communication) . Asmall subsurface chlorophyll a maximum was presentbetween 3 and 12 m in depth throughout the study,except during the spring and during the diatom bloomin October (Fig . 4) .
Carbon and nitrogenThe total particulate organic carbon (POC) and nitro-gen (PON) content varied considerably and followed ageneral decrease from spring to fall, except for a singlesample on 10 July (Fig . 3C). At all depths, regressionsof POC to chlorophyll a indicated that POC increased(p<0.0003) with the biomass of the small phytoplank-tonic cells . POC was also positively related to thephytoplankton biomass of the large size classes, butless strongly (p>0.005; Table 1) . The intercepts of theregressions of POC to chlorophyll a differed from 0 for
Fig. 1. Location of sampling site in Baie des Chaleurs, Quebec .
149
all size fractions and all depths (Table 1) . This indicatesthat a significant portion (ca 60%) of total particulateorganic matter in the water column was material otherthan phytoplankton. Regressions of POC to PON weresignificant for all three size fractions (p<0 .05) and thecorrelation coefficients (r2 ) for particles measuring 0.7to 5, 5 to 20 and >20 µm, were 0 .84, 0.50, and 0.57,respectively (Fig . 5). Both C/N ratios and their vari-ances increased with the size of the particles : the meanwas 7.53 (U2 = 1.58) for <5 µm particles comparedto 8 .29 (0. 2 =74.38) for 5-20 am particles and 12 .84(v.2 = 118.36) for >20 µm particles .
Structure of the water columnFrom May until August 1989, a warming at the sur-face lead to a progressive stratification of the watercolumn. Then, from August to December the watercolumn became progressively homogenized and inmid November the temperature returned to near 0 °C(Fig. 4). The Brunt-Vailsala index of stability of thewater column (N2) was intermediate during June andJuly, increased sharply in early August, decreased inlate August and then remained low from September toDecember (Fig . 2C) . This index was generally greater
150
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35-30-
20-
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5-0
A
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DFig. 2. Seasonal changes in (A) integrated chlorophyll a, (B) percentage of chlorophyll a in the small fraction (<5 µm) to the total amount,and (C) the Brunt-Vaisala stability index of the water column at Gascons, Baie des Chaleurs, during the summer 1989 .
between 3 and 15 m than between 15 and 21 m, indi-cating a larger density gradient in the upper part of thewater column . Drops of the stability index indicatedperiodic destabilizations of the vertical structure of thewater column, for instance in early July and in lateAugust (Fig. 2C) .
The mass of particulate organic carbon and chloro-phyll a (<5 µm) was correlated (p<0 .05) withthe structure of the water column (Table 2) . Thestanding crop of 0.7-5 pm cells tended to increasewith increased stability and stratification . In contrast,chlorophyll a and POC levels for large cell fractionswere not correlated with the stability of the water col-umn .
The extinction coefficient (k') attained a maxi-mum during the spring and subsequently decreased,
I
although with marked fluctuations (Fig . 6). Phyto-plankton biomass in the upper 9 m of the water columnaccounted for 46% of the variations (Fig . 6) . The depthof the photic zone (1 % surface irradiance) first declinedto the depth of the study site (25 m) in late August .
Discussion
A striking feature of the phytoplankton community inthe Baie des Chaleurs is the abundance of picoplank-ton (<5 µm) during summer and autumn . These smallcells were not detected in the earlier study by Brunel(1962) who sampled phytoplankton with a net (cells>20 ftm were collected) . Recent studies using othertechniques have revealed communities dominated by
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picoplankton in many types of environments (Johnson& Sieburth, 1979; Waterbury et al., 1979; Jochem,1988 ; Jochem, 1989) . A dominance by small cellsis usually associated with strong stratification (Leg-endre & Le Fevre, 1991) and has been reported foroligotrophic oceanic waters. It has also been foundin lagoons with low levels of nutrients (Klaveness,1990) and in shallow well-mixed regions (Roy et al.,1991). The stratification during summer in the Baie desChaleurs is caused by a high heat flux at the surfacecombined with weak tidal forcing (Bonardelli et al.,1993). We can relate the dominance of the picoplank-ton to the stability of the water column at differenttime scales. On a large scale (months), the percentagechlorophyll a in small cells (<5 µm) varies in par-allel with the seasonal temperature change (Fig . 2B)whereas on a shorter time scale (days), the biomass ofultraplankton is strongly correlated with fluctuations
A S 0 N
- fill
5)) TL
- 40 00 fV
-30
EE
-20 41
-10
a)d
0C
1 5 1
Fig . 3 . Seasonal changes in (A) integrated chlorophyll a in three size fractions, (B) total organic particulate carbon in three size fractions and(C) total integrated chlorophyll a and particulate carbon at Gascons, Baie des Chaleurs, during the summer 1989 .
in the Brunt-Vailsala stability index . We did not makecounts of phytoplankton species present during ourstudy and thus cannot state which species accountedfor the dominant <5 µm fraction. They were possiblysmall flagellates, since Roy et al. (1991) observed thatthese dominated the phytoplankton measuring < 10 smduring the summer in the Magdalen Islands, in thecentral Gulf of St. Lawrence. Such cells (certainly thelarger species) are capable of vertically migrating toareas of increased nutrients at greater depths (Jochem,1989; Yamazaki & Kamynowski, 1991) and thus arewell adapted to stratified waters . Further, because oftheir high surface area to volume ratio, small cells gen-erally have an increased ability to procure nutrients innutrient limited environments (Raven, 1986) . In con-trast, the picoplankton that dominate in ChesapeakeBay, are mainly cyanobacteria (Synechococcus) andchlorophytes (Marshall & Lacouture, 1986) . Studies
152
Chlorophyll a (mg m-3)
Temperature ( °C)
Fig. 4. Seasonal changes in the depth distribution of chlorophyll a and temperature at Gascons, Baie des Chaleurs, during the summer 1989 .
on seasonal and regional distribution of Synechococ-cus indicate that these cyanobacteria grow less wellat temperature of <10 °C (Murphy & Haugen, 1985 ;Jochem, 1988) and thus would be restricted to theperiod of August in Baie de Chaleurs . Margalef et al.(1979) indicate that dinoflagellates are also highly sen-sitive to changes in the structure of the water column .Larocque & Cembella (1991) sampled at Gascons dur-ing our study (1989) and report that dinoflagellateswere abundant in summer. However, most measured5-10 pm in size and thus were larger than the dominantfraction in our study.
Because of the difficulty of sampling during win-ter, due to ice cover, our observations were made fromearly spring to late fall . This period covers most of theannual phytoplankton production cycle . In ice-covered
environments, the spring bloom normally developsrapidly once the ice disappears (Sakshaug & Skjoidal,1989). Our samples in May 1989 recorded the endof the spring bloom . At this time, chlorophyll a lev-els peaked and large cells dominated . Spawning ofthe green sea urchin Strongylocentrotus droebachien-sis near Gascons in late April 1984, as documentedby Starr et al. (1993), provides further evidence ofthe timing of the spring bloom in our study area, asthe urchin spawns in response to metabolites releasedfrom the spring diatom bloom (Starr et al., 1990) .We probably missed the onset of the spring bloomby a couple of weeks. The fall bloom was brief andprobably localized, since it was detected on only onedate. The major species were the diatoms Skeletonemacostatum and Leptocylindricus danicus. In controlled
40 -
30-
20 -
10-
00
0
< 5 pin
50 100
microcosm experiments by Marasse et al. (1989), thelatter diatoms were also bloom species and small flag-ellates measuring <7 am became dominant after thebloom. This further suggests that small flagellates aremajor species in the postbloom phytoplankton com-munity in the Baie des Chaleurs .
Chlorophyll a levels in our study (10-20 mg m-2)were similar to those recorded elsewhere in the Gulfof St. Lawrence (Sevigny et al., 1979; Hargrave et al.,
00Z-0
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150 200 250
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Particulate Carbon (g m"3)Fig . 5. Relation of particulate nitrogen to particulate carbon for three size fractions at 9, 15 and 21 m in depth . The values marked by anasterisk (*) indicate samples taken during the diatom bloom on 28 October 1989 .
1985 ; Vandevelde et al., 1987) but considerably low-er than those reported for more southern embaymentssuch as Narragansett Bay (Durbin & Durbin, 1981) .The progressive decrease in chlorophyll a levels dur-ing the summer and autumn in the Baie des Chaleurs isconsistent with a nutrient regenerated system . In suchsystems, primary production relies mainly on nutrients,particularly nitrogen, which are recycled through sev-eral trophic levels . Goldman's (1988) model of pelag-
154
A
0 0.2
0.4
0.6
0.8
I
1 .2
1 .4
1 .6
Chlorophyll a (rug rn-3)
is systems indicates that short food chains based onlarge phytoplanktonic cells are required for significantexport of organic matter to higher trophic levels andthat energy from small phytoplankton cells is most-ly lost to microbial organisms . In the microbial foodweb, small heterotrophic flagellates consume bacte-ria and are in turn exploited by the microzooplanktonbefore entering the food chain of larger animals (cope-pods, larvae, fishes) . Although total respiration loss-es increase with the number of trophic levels (Azamet al., 1983), a small percentage of nutrients is eventu-ally exported from the system towards higher trophiclevels or lost through sedimentation . In either casethe total amount of nutrients available through regen-eration tends to decrease . Thus, additional sources ofnutrients are required to maintain or increase the stand-ing crop of primary producers .
1 .8
-0
-10
C.as
- 20 c.e0a
- 30
40
Fig. 6 . Relationship between the attenuation coefficient k' and the chlorophyll a content in the upper layer of the water column (A) and seasonalchanges in the attenuation coefficient k' and the depth of the photic zone at Gascons, Baie des Chaleurs, during the summer 1989 (B) .
To examine the potential contribution of tidalmixing as an enrichment process, we calculatedthe Simpson-Hunter coefficient (Simpson & Hunter,1974) :
hS = log to CdU3'
where h = depth of the water column ; U= average tidalvelocity ; Cd = bottom friction
The calculated value indicates that mixing of thewater column at Gascons during the summer wouldrequire an average tidal current of >30 cm s -1 . Sincethis velocity is five times greater than the averagevelocity at Gascons (Bonardelli et al., 1993), tidalmixing probably contributes little to nutrient enrich-ment .
Table 1 . Regression equations, determination coefficients(R2) and significance levels (p) for regressions of particulatecarbon to chlorophyll a for three size fractions at 9,15 and
Table 2 . Pearson's correlation coefficient (r 2 ) between theBrunt-Vaisail5 index of stability of the water column (N) andchlorophyll a and particulate organic carbon in three size frac-tions at 9, 15 and 21 m in depth .
* = Significant at the 0 .05 level . ** = Significant at the 0 .01 level
The stability indices show that stratification wasperiodically disturbed (Fig . 2) . Such events have beensuggested to enhance phytoplankton production in sta-ble environments through nutrient enrichment (Legen-dre et al., 1982; Legendre & Demers, 1984 ; Demerset al., 1986). We cannot state whether these destratifi-cation events were due to mixing of the water columnor to advection by upwellings . Bonardelli et al. (1993)
1 55
report periodic wind-driven upwellings at approxi-mately 7 d intervals throughout the summer at Gas-cons. Although these upwelling events could causesome nutrient replenishment in the upper photic lay-er leading to increased phytoplankton growth duringthe ensuing period of stratification (as in other temper-ate coastal embayments), in situ nutrient regenerationmust account for most of the demands for primary pro-duction (Hargrave et al., 1985). The short durationof the wind-driven upwellings in Baie des Chaleurslasting for 1-3 days (Bonardelli et al ., 1993), whichcorrespond mostly to a offshore flow of the surfacelayer and inshore flow of the bottom layer would notlikely provide any significant mixing of the two lay-ers to affect the nutrients richness in the photic zone(LeQuere, 1992) .
Other factors, such as grazing, may also affectnutrient regeneration and the structure of the phyto-plankton community. Little information is availableon the impact of grazers at Cascons . The report byLacroix & Filteau (1969) and observations duringAugust and September 1991 (Y . Lagadeuc, UniversiteLaval, personal communication) show that the den-sity of grazing copepodes and copepodites in Baiedes Chaleurs often exceeds 2 .0 x 104 m-3 . In addi-tion, in September-October, average values of 5000bivalves larvae m-3 have been observed by Raby et al.,(1994). If these organisms ingest phytoplankton at therate of only 10-9 g chlorophyll a d-1 ind' (Kiorboe& Mohlenberg, 1985), up to 20% of the standingcrop could be consumed daily . The high abundanceof zooplankters indicates that they could substantiallycontribute to the regeneration of nutrients (Harrison,1980) .
The positive correlation of phytoplankton abun-dance with the stability of the water column, the abun-dance of small particles and the C/N ratios of smallparticles suggest that a microbial food web dominatesthe ecosystem at Gascons during the summer. Low C/Nratios for small particles (7 .4) and the high interceptof the regression between chlorophyll a and particu-late carbon suggest that small cells such as flagellates,ciliates, or bacterioplankton are abundant. The stabil-ity of these C/N ratios over time indicates that thecomposition or origin of small particles varies onlyslightly from May to October. In contrast, the morevariable C/N ratios for larger particles suggest het-erogeneous origin or composition. The relative abun-dance of different phytoplankton species undoubtedlychanges seasonally and the thick cellulose cell walls(theca) of some species (dinoflagellates for example)
21 m in depth .
Depth (m) Regression equation R2 P
<5 g.m
9 y = 106 .0 + 174.0 x 0 .50 <0.00011 _5 y = 112 .6 + 161 .4 x 0 .42 0 .000321 y = 97 .4 + 176.7x 0 .74 <0.0001
5-20 gm
9 y = 22 .5 + 51 .1 x 0 .23 0.006815 y = 22 .0 + 101 .8 x 0 .21 0 .003521 y = 32 .6 + 55 .5 x 0 .16 0 .035
>20 gm
9 y = 18 .9 + 81 .7 x 0 .25 0.007215 y= 14.9+ 38.7x 0 .14 0.04921 y = 16 .8 + 24 .8 x 0 .10 0 .10
Variable Correlation coefficient9 m 15 m 21 m Integrated
may explain high levels of particulate carbon whenthese species are abundant (Haug et al., 1973). TheC/N ratios during the diatom bloom in late Octoberwere near the higher limit recorded for the >20 µmsize fraction and considerably increased the overallvariance for this group (Fig . 5) .
During the summer and autumn in Baie desChaleurs, the ecosystem remains dominated by smallcells, even though periodic destratification of the watercolumn caused by coastal upwellings may enrich sur-face waters. The abundance of small-sized particulatematter with low and stable C/N ratios and the gener-al decrease in phytoplankton biomass over the sum-mer suggests that a large part of the phytoplanktonbiomass is supported by nutrients regenerated througha microbial loop . Studies of primary production andof nutrient availability at small time scales (days), andexperiments examining the effect of grazing by micro-zooplankton and zooplankton, are required to elucidatemechanisms causing the unusual duration of the periodof dominance by picoplanktonic cells .
Acknowledgments
We are indebted to Aquatek Mariculture Inc . and itspersonnel for assistance throughout the period of sam-pling in the field and to K . Drinkwater, P. Harrison andF. Jochem for critical comments on the manuscript . Theproject was supported by NSERC and OPEN fundingto J.H.H .
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