The western North Atlantic bloom experiment

Deep-Sea Research II. Vol.40. No. 1/2,pp. 279-305. 1993. Printed in Great Britain.

0967~)645/93 $5,00+ 0.00 PergamonPressLtd

The western North Atlantic Bloom Experiment W. G. HARRISON,* E. J. H. HEAD,* E. P. W. HORNE,* B. IRWIN,* W , K . W . LI,* A . R . LONGHURST,* M . A . PARANJAPEt a n d T. PLAIT*

(Received 13 May 1991; in revised form 1 January 1992; accepted 20 March 1992)

Abstract--An investigation of the spring bloom was carried out in the western North Atlantic (40-50°W) as one component of the multi-nation Joint Global Ocean Flux Study (JGOFS) North Atlantic Bloom Experiment (NABE). The cruise track included an extended hydrographic section from 32 to 47°N and process studies at two week-long time-series stations at 40 and 45°N. Biological and chemical data collected along the transect indicated that the time-series stations were located in regions where the spring bloom was well developed; algal biomass was high and surface nutrient concentrations were reduced from maximum wintertime levels. Despite similarities in the vertical structure and magnitude of phytoplankton hiomass and productivity, the two stations clearly differed in physical, chemical and other biological characteristics. Detailed depth profiles of the major autotrophic and heterotrophic microplankton groups (bacteria, phytoplankton, microzooplankton) revealed a strong vertical coherence in distribution at both sites, with maximum concentrations in the upper 50 m being typical of the spring bloom. Ultraplankton (<10 um) were an important component of the primary producers at 40°N, whereas larger netplankton (diatoms, dinoflagellates) were more important at 45°N. Silicate depletion was clearly evident in surface waters at 45°N, where diatoms were most abundant. Despite the relative importance of diatoms at 45°N, dinoflagellates dominated the biomass of the netplankton at both sites; however, much of this community may have been heterotrophic. Bacterial biomass and production were high at both stations relative to phytoplankton levels, particularly at 45°N, and may have contributed to the unexpectedly high residual ammonium concentrations observed below the chlorophyll maximum layer at both stations. Microzooplankton grazing dominated phytoplankton losses at both stations, with consumption as high as 88% of the daily primary production. Grazing losses to the mesozooplankton, on the other hand, were small (< 10%), but mesozooplankton contribution to the vertical flux of organic matter (fecal pellets) was important at 45°N. F-ratios estimated by 15N tracer methods and sediment trap fluxes were similar and suggested that - 3 0 % of the daily primary production was lost by direct sedimentation during the observation period. Numerous similarities in bloom characteristics were noted between the western and eastern Atlantic study sites.

INTRODUCTION

SATELLITE remote sensing methods have clearly established the spring phytoplankton "bloom" in the North Atlantic to be one of the most prominent variable features of the global ocean color field (BROWN et al., 1985; ISAIAS et al., 1986; LEWIS, 1989). Furthermore, it has become evident that the growth cycle of ocean biota strongly influences the exchange of CO2 between the atmosphere and the surface ocean (e.g. TAYLORet al., 1991). *Biological Oceanography Division, Bedford Institute of Oceanography, Box 1006, Dartmouth, Nova Scotia B2Y 4A2, Canada. tNorthwest Atlantic Fisheries Centre. Box 5667, St. John's, Newfoundland A1C 5X1, Canada. 279

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These, among other considerations, were the bases for selecting the North Atlantic Bloom Experiment (NABE) as the first of many multination investigations of biogeochemicat processes planned under the JGOFS program (DucKLOW, 1989; SCOR, 1990a,c). This large-scale process study was centered in the eastern Atlantic along 20°W longitude at 33. 47 and 60°N, and covered the period March-September 1989 (DucKLOW, 1989). The Canadian component of NABE took place considerably further west (40-50°W), providing an opportunity for large-scale (> 1000 km longitudinal separation) comparative' studies of bloom processes at similar latitudes and times of year on opposing sides of the North Atlantic basin. Objectives of the Canadian cruise were to establish initially from survey work one ~,r more representative sites from which detailed studies could be made of carbon biomass and cycling of the major planktonic components of the spring bloom. Experimental work focussed on the productivity and distributional relationships of autotrophs and micrt~heterotrophs and the nature and magnitude of losses of biogenic carbon from the euphoric zone, including zooplankton grazing and passive particle sinking. We report here some of the major hydrographic, chemical and biological features of the western North Atlantic spring bloom during the period mid-April to mid-May 1989.

METHODS

Sampling JGOFS studies were carried out as part of the CSS BAFFIN western North Atlantic cruise 89-003 during the period 20 April-18 May 1989. The sampling strategy was designed around an initial meridional transect, beginning in the subtropical gyre (32°N) east of the main eddy field of the Gulf Stream and just north of Bermuda (Fig. 1) and proceeding

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north, to establish an "optimum" location for the planned process studies of the spring bloom. Continuous measurements of in vivo fluorescence (Turner Designs), temperature and salinity (Guildline) were made using surface ( - 4 m) seawater from the ship's intake system and logged, along with position and time (GMT), on a portable computer. Discrete samples were collected using a rosette-style sampler equipped with 18 8-1 PVC sampling bottles, a CTD (Guildline), fluorometer (Aquatracka) and 4 Jr light meter (LI-COR SPH). Sampling was confined to the upper 200 m. Time-series measurements were made at two locations: 40°N, 47°W from 27 April to 4 May, and 45°N, 41°W from 8 to 13 May (Fig. 1). At these stations, rosette samples were collected twice daily, in the morning (-0800h local time) and at sunset (1900-2000 h). Actual sampling locations were determined by the positions of free-floating sediment trap arrays deployed at the beginning of each of the time-series studies. Strict adherence to JGOFS recommended sampling procedures, i.e. "ultra-clean" techniques (SCOR, 1990b) could not be followed, but our rosette bottles, incubation vessels (see below) and other containers were thoroughly cleaned (dilute HCL) and rinsed (demineralized water) before the cruise; periodic acid cleaning and daily rinsing also were done at sea. The rosette bottles were custom designed (Crooks Mechanical Systems, Dartmouth, Nova Scotia) to circumvent toxicity from latex rubber: the need for internal springs was avoided by adopting an external closing mechanism. Furthermore, the closure seals were made of Teflon. Despite these precautions, however, metal contamination in our productivity experiments was evident (J. MARTIN, personal communication), although detrimental effects were not apparent based on comparisons of our primary productivity values with those where contamination was minimal. Other core measurement protocols followed JGOFS recommendations (see below). Hydrography, nutrients and particulates

Temperatures, salinity and depth were measured using a Guildline CTD. Inorganic nutrients were collected from the rosette bottles (or Niskin bottles in the case of productivity experiments, see below) and measured either by automated methods (NO3, PO4, SiO3) using an Alpkem RFA autoanalyser or manually (NH4) using the standard hypochlorite method of SOLORZANO(1969). All nutrient analyses were done immediately after sample collection; NH 4 samples were prefiltered through a glass-fiber filter (Whatman GF/F) before analysis. Particulate organic carbon (POC) and nitrogen (PON) were determined by high-temperature combustion (Perkin-Elmer Elemental Analyzer) of samples concentrated on precombusted GF/F filters. Hydrography, nutrients and phytoplankton biomass (chlorophyll a) were measured at all stations, whereas abundance of other plankton forms and rate process measurements (see below) were concentrated at the time-series stations at 40 and 45°N. Phytoplankton pigments and cell counts

Phytoplankton pigments were measured by standard fluorometric methods and by HPLC. Chlorophyll a (Chl a) and phaeopigments were determined on acetone extracts of replicate (100 ml) samples collected on glass-fiber filters (Whatman GF/F). The fluorometric method of HOLM-HANSEN et al. (1965) was employed using a Turner Designs instrument. Additional Chl a samples were collected occasionally for size-fractionation (using Nuclepore membrane filters; IRWINet al., in press) to assess the relative importance

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of the < 1 pm and > 1 pm size fractions. For HPLC analysis, water samples ((}.5-1.5 1) were filtered onto glass-fiber filters, which then were frozen in liquid nitrogen and stored in the dark at - 2 0 C for later analysis ashore. Immediately before being run, samples were ground in 1 ml 90% acetone-water, using a Teflon-glass homogenizer. The glass fibers were removed by centrifugation (2 rain at 12,000 g). The samples were then diluted 1:2 with aqueous ammonium acetate (0.5 M) and 250 pl of the mixtures were injected onto a Beckman C-18 3#m Ultrasphere reversed-phase column (4.6 x 70ram). The samples were run using a gradient elution system of aqueous ammonium acetate-methanol (20:80) as solvent 1 and ethyl acetate-methanol (30:70) as solvent 2. The gradient was run over 15 min from 0 to 100% solvent 2. Eluting pigments were detected using a Beckman 167 UV-vis scanning detector set at 430 nm. Peaks were generally identified by comparisons ol their retention times and those of standards obtained from Sigma Chemical Co. (chlorophylls a and b) and Dr R. Bidigare (chlorophyll c and most carotenoids). Alpha-carotene was identified by comparison of its retention time with a peak found in a culture of prochlorophytes provided by Dr F. Partensky. Relative concentration units, given in the results, are the relative areas under the peaks in absorbance traces. According to BIDIGARE et al. (1990), "primary taxonomic markers" fucoxanthin, peridinin, prasinoxanthin. zeaxanthin, 19'-hexanoyloxyfucoxanthin and chlorophyll b indicate the presence of diatoms, photosynthetic dinoflageltates, prasinophytes, coccoid cyanobacteria, prymnesiophytes and "green" algae, respectively. Prochlorophytes may be distinguished by "alpha-carotene and divinyl chlorophyll a-like" pigments (CHISHOLMet al., 1988). In addition to pigments, samples were collected for cell counts by direct microscopic analysis or by flow cytometry. Phytoplankton cells were enumerated by light microscopy from samples for microzooplankton (see below). Cells were settled from 50 or 10(I ml aliquots and were identified and counted with a Zeiss inverted microscope (HASLE, 1978). Cell volumes were estimated by assigning the appropriate geometric cell shapes (Ro'H, 1981), and organic carbon content was calculated by the relations of STRATHMANN(1967) for diatoms and other phytoplankton. Unicellular cyanobacteria were enumerated by epifluorescence microscopy (LI et al., 1992). Other autofluorescent plankton were determined by flow cytometric analysis that differentiated two groups of phytoplankton: the photosynthetic nanoplankton (PNAN), red-fluorescing cells with or without phycoerythrin in the size range >2/~m but < i0/~m equivalent spherical diameter (ESD), and the "very small red-fluorescing cells" (VSRF), red cells lacking phycoerythrin and in the size range <2 #m ESD. Thus, the < 10 #m phytoplankters include the cyanobacteria, PNAN and VRSF cells and will be collectively referred to as ultraplankton; methodological details are given by LI et al. (1993). Heterotrophic bacteria, m i c r o z o o p l a n k t o n and m e s o z o o p l a n k t o n abundance

Heterotrophic bacteria were enumerated by epifluorescent microscopic examination of DAPI-stained cells concentrated on 0.2 #m black polycarbonate (Nuclepore) filters (Ll et al., 1993). Samples for microzooplankton were collected by following JGOFS protocols. Three types of samples were coUected from each depth. (1) A 50 ml sample from the rosette bottles was fixed in 2% filtered gluteraldehyde, stained with DAPI (PORTER and FEI(;, 1980) andfiltered through a 0.8 pm pore size black Nuelepore filter and mounted in lowfluorescence immersion oil on a glass slide and kept frozen at -20°C until they could be

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counted (BLoEM et al., 1986). This sample was used to enumerate heterotrophic and autotrophic pico- and nanoflagellates by epifluorescence. (2) A 500 ml whole water sample was fixed with 1% alkaline Lugol solution and preserved with 1% buffered formaldehyde. This sample was used to enumerate ciliates and other protists (as well as phytoplankton) by light microscopy. (3) A 20 1 whole water sample was gently filtered through a 30/~m mesh, concentrated to a final volume of 500 ml and preserved with alkaline Lugol and formaldehyde as above. This sample was used to enumerate sarcodines and small metazoa. In this report, results from the first two types of samples are discussed. The frozen slides were examined for heterotrophic and autotrophic nanoflagellates on a Zeiss epifluorescence microscope equipped with a 50 W mercury lamp and appropriate filter combinations. At least 100 cells per slide were counted. Flagellates were measured with an eyepiece reticule and volumes were estimated by assuming sphere or prolate spheroid shapes. The numerical abundance of ciliates was estimated from the whole water samples by methods described in PARANJAPEet al. (1985) and PARANJAPE(1988). A 50 ml aliquot was allowed to settle and was examined with a Zeiss inverted microscope. Biovolumes of various taxa were estimated by assuming simple geometric shapes or combinations of shapes. Mesozooplankton densities were determined using the BIONESS multiple opening/ closing net sampler (SAMEOXO et al., 1980). At 40 and 45°N, daytime and nighttime BIONESS tows were made to 500 m, divided into 16 and 19 depth intervals, respectively. Dry weights were determined for two size fractions: >1 mm and <1 mm but <200 urn. Samples representing the <200 ,urn fraction were not taken. Zooplankton were sorted and enumerated to the level of genus or species, depending on their abundance in the tows.

Carbon biomass conversions

To facilitate comparison of stocks among the various plankton groups investigated, abundance estimates were converted to carbon biomass using established relationships based on either C/cell and C/cell volume (Table 1). For "total" phytoplankton, based on Chl a levels, a conversion factor of 40 (C : Chi a) was used. LI et al. (1993) discuss the rationale for the selection of this factor.

Phytoplankton and bacterial productivity

Primary productivity was measured by the 14C method employing m situ incubations (SCOR, 1990b). Samples were collected daily at the time-series stations before dawn from 11 depths in the upper 100 m using 12 1 Niskin bottles. Samples were recovered at sunset (-12 h later), filtered onto GF/F glass filters and processed for radioactivity analysis by liquid scintillation spectrometry. As in the case of Chl a, parallel samples were sizefractionated (post-incubation) on a number of occasions to assess the contributions of the <1 /~m and >1 #m size fractions to the total productivity. "New" productivity was estimated by the uptake of aSN-labeled nitrate (DUGDALEand GOERING, 1967). To 500 ml samples collected from 8-10 depths in the upper 100 m, 15NO3 (99 atom %) was added at 10% ambient nutrient level and incubated on deck for 2-4 h in perforated screen boxes

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Table 1. Biomass (carbon) conversion ]hctotw and calculations. Living biomass comprised oj heterotrophw bacteria (BACT), phytoplankton, other microheterotrophs (MICROHET) and mesozooplankton (MESO ~ ZOO PL ). Phytoplankton are further subdivided into uhraphmkton ( VSRF, CYANO, PNAN; Llct al., 19931and netplankton. Microheterotrophs subdivMed into heterotrophic flagellates (HNAN), oligotrictTs (OLIGO) and tintinnids (TINT). TPC = total particulate carbon, A UTOC = autrotrophic carbon, HETERO(" = heterotrophic carbon, DETC = detrital carbon

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Reference

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C:Chl a = 40 (kl et al., 1993).

to simulate natural light levels; both daylight and night incubations were done (SCOR, 1990b). Isotope enrichment of the particulates was determined by emission spectrometry (FIEDLER and PROKSCH, 1975). Daily (24 h) uptake rates were derived from the summed products of the daylight and dark hours and their corresponding 15NO3 uptake rates; dark uptake rates averaged 54% of the daylight rates. Bacterial productivity was estimated by 3H-thymidine and 3H-leucine incorporation; L~ et al. (1993) provide procedural details and carbon conversion factors required to convert rates of radioisotope incorporation into rates of bacterial production. Micro zooplankton grazing

Microzooplankton grazing was determined by the ',dilution method" first described by LANDRV and HASSErr (1982), Seawater was collected from 10 m with a 30 1 Niskin bottle. Particle-free seawater (cf. LI, 1986)was prepared by passing water through 55 mm dia Whatman GF/F filters. Several proportions of filtered and whole seawater were prepared and dispensed into acid-cleaned, 2 1 polycarbonate bottles in duplicate. As ambient nutrients were relatively high, additional nutrients were not added. Bottles were incubated on deck in acrylic incubators cooled with running surface seawater and screened with R o h m and Haas blue Plexiglass filters (No. 2069; LAws et al., 1989) to simulate the submarine illumination at the depth of collection. Experiments were run for 24 h. Samples for Chl a, dissolved nutrients and microplankton abundance were taken from

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all experimental bottles at the beginning and at the end of incubations. We also ran true controls (100% filtered seawater) to monitor leakage and subsequent growth of autotrophic cells during incubation (LI, 1990); these were also treated in a similar manner as the experimental bottles. We did not detect any Chl a, assayed by fluorometry, in the filtered seawater before or after incubation, nor did we detect the presence of autotrophic cells by light microscopy. Microzooplankton were enumerated as described earlier. The growth rates of phytoplankton and grazing rates on them were calculated as described in previous work (PARANJAPE,1987, 1990). Mesozooplankton grazing, defecation and excretion rates Daily pigment defecation rates were calculated for individual copepod species or groups of species by measuring gut evacuation rates in incubation experiments, using copepods either >505 ~m or between 200 and 505/~m, in filtered seawater every 4 h for 24 or 48 h. Initial rates in these experiments were averaged over either night or daytime periods, if the two were different. They were then summed over the densities of individual species or groups of species in the mixed layer of the water column during either the night or the day to give community nighttime, daytime and hence 24 h pigment defecation rates. Community carbon defecation rates were derived from community pigment defecation rates by measuring the carbon-pigment ratio in fecal pellets collected from copepods (>505/~m), which had fed in situ and which were allowed to defecate for 3 h in filtered seawater (SCOR, 1990b). The fecal pellet collection experiments were carried out during the day and at night, but no substantial differences were seen in the ratio at different times of day, so that only one carbon-pigment conversion factor was used: factors were - 170 at 40°N and - 3 0 0 at 45°N. Grazing rates were estimated from defecation rates as follows. Firstly, the fraction of ingested pigment, which was destroyed during passage through copepod guts, was measured. This was done either by looking at total pigment budgets during in vitro grazing experiments, using copepods which had been starved for 12 h prior to feeding, or by comparing ratios of pigment to a conservative tracer (biogenic silica, CONOVERet al., 1986) in food and feces in these same feeding experiments. Ratios of pigment-silica in pellets from copepods, which had fed in situ, were also compared with those of particulate material in the water column to demonstrate that the in vitro results were consistent with apparent degrees of pigment destruction in situ. Using median values for these estimates of the degree of pigment destruction ( - 5 0 - 7 0 % ) , pigment grazing rates were calculated. Equivalent phytoplankton carbon grazing rates were then calculated from these by using the appropriate C:Chl a conversion ratio (i.e. 100:1). Excretion rates were measured in the same time-course incubation experiments in which gut evacuation rates were measured. Ammonium concentrations were measured in seawater from which copepods had been screened, using the method of 8OLORZANO (1969). The time courses of ammonium accumulation were fitted to curvelinear plots (HEADe t al., 1988) and the initial rates were used together with estimates of the total numbers of copepods in the incubations to give "average individual" excretion rates. These were converted to daily community rates by multiplying by the total copepod densities (similar to the method used above for community defecation rates, except that the contributions of individual species could not be evaluated).

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Sediment traps

Free-floating sediment traps of the MULTI-TRAP design (KNAUER et al., 1979) were deployed at the beginning of each time-series station and followed for the duration of the station work. Four trap tubes were positioned at each of three depths: 150,250 and 500 m ', recoveries were after 163 h at 40°N and 92 h at 45°N. Trap contents were pooled for a particular depth and analysed for POC, PON and pigments (Chl a, phaeopigments) after "swimmers" were removed. Only results from the 150 m traps will be discussed. RESULTS

N - S transect

The continuous record of in vivo fluorescence and salinity/temperature from the ship!s seawater intake system revealed a number of interesting features in the N-S transect (Fig. 2). Most prominent were: (1) strong property transitions, particularly at ~37°N, (2) maximum surface fluorescence in the 40--45°N region, and (3) marked variability in properties in the region of the 40°N time-series station compared with the 45°N station; fluorescence and temperature were highly (inversely) correlated. Although not as well resolved spatially, seven hydrographic stations occupied along the transect provided a 22

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more complete (three-dimensional) picture of the N - S hydrography, nutrient and phytoplankton biomass fields (Fig. 3). Noteworthy were similarities in N O 3 and temperature distributions, showing a - 3 8 ° N transition clearly through the 200 m depth contour, and the relationship between the Chl a distribution and NO3. Maximum N - S gradient in Chl a concentrations coincided with the surface "outcropping" of the 18°C isotherm and the 1 mmol m 3 NO3 contour ( - 3 8 ° N ) ; highest recorded surface Chl a concentrations (at - 4 0 and - 4 5 ° N ) coincided with surface depressions in NO3 concentration. Note that the apparent latitudinal differences in the property transition zones in Figs 2 and 3 (i.e. 37 vs

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38°N) originated from the software used to contour the data in Fig. 3. The location indicated in Fig, 2, therefore, is probably more accurate. A T - S analysis of the transect data was made using ARMI and BRAV'S (1982) algorithm for western North Atlantic water to help characterize the water mass composition, particularly at the sites of the two time-series stations (Fig. 3). Two important features were revealed from this analysis: firstly, the ~38°N transition was clearly evident, and secondly, a very strong negative salinity anomaly was seen in the near surface water~ (<100 m) centered at 45°N. The large negative salinity anomaly is characteristic of waters originating from the Labrador shelf, some 1500 km to the west (J. LAZIER, personal communication), Time-series stations

Small scale variability in chemical and biological properties was apparent over the course of the week long studies at both time-series stations, although the general vertical structure persisted (Figs 4 and 5). Integrated Chl a (0-50 m) tended to decrease with time at both stations; integrated NO3 concentrations showed no clear temporal pattern at 40°N but tended to decrease with time at 45°N. LI et al. (1993) discuss changes in ultraplankton and bacterial populations at the time-series stations. Other components of the plankton were not sampled frequently enough to discern temporal trends. Temperature, density and NO 3 profiles indicated a weak mixed-layer in the upper 25-40 m (Fig. 6). Biological consumption of NO3 at both stations was significant but not complete since surface concentrations were still - 2 mmol m -3 (maximum wintertime concentrations - 1 0 mmol m-3: GLOVERand BREWER. 1988). Similarities also were seen in the magnitude and vertical distribution of phytoplankton biomass (Chl al and primary productivity at the two stations although the Chl a layer extended somewhat deeper al 45°N than at 40°N (Figs 4.5 and 7). Primary productivity profiles indicated a euphoric zone of - 5 0 m at both stations. Surface Chl a levels ( ~ 2 mg m -3) and column productivitie~ (~1 g C m -2 day - 1) were indicative of oceanic bloom conditions. Beyond these similarities, the stations differed considerably with regard to other physical/chemical and biological properties. The most notable difference in the chemistr~ of the two stations was the near surface depletion of silicate at 45°N. which had not occurred at the more southerly station (Fig. 8), suggesting that diatoms were a morc important component of the phytoplankton at the northerly station. Indeed. pigment analysis and floristics supported this view. H P L C pigment analysis showed the prevalence of diatom pigments at 45°N. while the 40°N analysis revealed a mixture of pigments found at 45°N and at the southerly most station at 32°N. but not at both (Fig. 9). Microscopic analysis revealed that diatoms were approximately an order of magnitude more abundant at 45°N than at 40°N, dominated by Rhizosolenia sp., Fragilariopsis sp., Thalassionema sp., Thalassiosira sp. and several species of Nitzchia. At both stations, major components of phytoplankton identified by light microscopy were diatoms, dinoflagellates, prymnesiophytes, cryptophytes and chlorophytes. Nearsurface samples contained filaments of Oscillatoria sp., presumably broken away from bundles or mats, but these could not be enumerated with precision. A! 40°N. phytoptankters ranged from 4 x 104 to 2 × 105 t -~ in the upper 50 m. Dinoflagellates and prymnesiophytes were dominant numerically with dinoflageUates accounting for >70% of the phytoplankton carbon biomass in the upper 100 m (Fig. 10). Despite the relatively

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Time on Station (h) Fig. 5. Near surface nitrate and Chl a concentrations at the 45°N time-series station, I,nits as m F'ig. 4. paralleled those of the bulk Chl a; highest levels were found in the upper - 5 0 m (Fig. 12) Ultraplankton carbon biomass at both stations was dominated by the nanoplankton, followed by the cyanobacteria and VSRF. Biomasses summed and compared with estimates based on Chl a showed that the ultraplankton accounted for virtually all of the phytoplankton biomass at the 40°N station but only about half at 45°N. [ J e t al. (1993) provide a m o r e detailed analysis of the ultraplankton at these stations. Heterotrophic bacteria were abundant at both stations (max: 2 × 109 cells 1 t Ll et al,, 1993). Vertical biomass distributions were similar to those of phytoplankton, i.e. maxim u m levels in the upper - 5 0 m (Fig. 12) although depth gradients were less pronounced, Bacterial carbon production in the upper 100 m represented only a small fraction ( - 12%) of the photosynthetic production at 40°N but made a much larger contribution (35-80%) at 45°N (see L~ et al., 1993, Table 2).

291

The western North Atlantic Bloom Experiment NO3 (mmol ~3) 0 I

TEMP (C) 10

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Fig. 6. Vertical profiles of temperature (7"), density (o0 and nitrate (NO3) at the two time-series stations (40°N, 45°N); mean values (horizontal bars = ± 1 S.D ). T h r e e g r o u p s of m i c r o z o o p l a n k t o n w e r e e x a m i n e d : h e t e r o t r o p h i c n a n o f l a g e l l a t e s ( H N A N ) , oligotrichs ( O L I G O ) a n d t i n t i n n i d s ( T I N T ) . N u m e r i c a l a b u n d a n c e a n d c a r b o n b i o m a s s of all t h r e e g r o u p s p e a k e d in the u p p e r 50 m like p h y t o p l a n k t o n and bacteria• T h e a b u n d a n c e of H N A N was a b o u t 1 x 106 1- t at b o t h stations, a n d t h e i r c a r b o n b i o m a s s r a n g e d f r o m 1 to 6 mg C m -3 in the m i x e d l a y e r (Fig. 12). M o s t H N A N w e r e in the size r a n g e 2 - 5 ,am. O l i g o t r i c h s a n d t i n t i n n i d s w e r e g e n e r a l l y m o r e a b u n d a n t at the s o u t h e r n station• O l i g o t r i c h a b u n d a n c e r a n g e d f r o m 1 x 103 to 5 x 103 1 1 at 40°N and 1 x 103 to 9 x 103 1 1 at 45°N. T i n t i n n i d s c o n t r i b u t e d little to n u m b e r s o r b i o m a s s at 45°N, while at 40°N t h e y r a n g e d f r o m 3 x 102 to 1.6 x 1031-1 . O l i g o t r i c h s c o n t r i b u t e d m o s t to the c a r b o n b i o m a s s at b o t h s t a t i o n s ; h o w e v e r , at the s o u t h e r n s t a t i o n their b i o m a s s (4-15 mg C m ~) was a l m o s t t w o - f o l d h i g h e r t h a n at the n o r t h e r n s t a t i o n ( 2 - 8 m g C m - 3 ) . T i n t i n n i d c a r b o n at the s o u t h e r n s t a t i o n r a n g e d f r o m 1 to 3 m g C m - 3 in the u p p e r 50 m and was in trace a m o u n t s at the n o r t h e r n station. S e v e r a l sizes of oligotrichs of the g e n e r a Strombidium, Lohmanniella, Tontonia a n d Halteria w e r e p r e s e n t at b o t h stations. L a r g e s t diversity of t i n t i n n i d species was o b s e r v e d at the s o u t h e r n station. Species of the g e n e r a Table 2. Mesozoopkankton carbon fluxes (retool m 2 day L) 40°N Grazing:

Carbon Nitrogen

4.71 0.54

Defecation:

Carbon Nitrogen

2.08 0.23

Excretion:

Nitrogen

0.19

45°N % Prim. prod. 5 4 % Trap flux 10 9 % NH4-uptake 2

9.14 1.12 13.84 1.54 0.31

% Prim. prod. 9 8 % Trap flux 104 73 % NHa-uptake 4

W.G. HARRISONet at.

292

C h l o r o p h y l l a (rag m 3)

Chlorophyll

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Fig. 7. Vertical profiles of Chl a and primary productivity at the two time-series station~: m e a n values (horizontal bars = t l S.D.). Dashed lines in u p p e r panels are m e a n a m m o n i u m (NH~) concentrations: values in lower panels are mean primary productivities integrated over the euphotic zone.

Ascampbelliella, Protorhabdonella, Amphorella, Codonellopsis, Eutintinnus, Climacocylis and Salpingella were most common, while at the northern station species of the g e n e r a Parafavella and Acanthostomella were present in small numbers. Microzooplankton grazing, measured by the dilution method at the beginning and at the end of the time-series station at 40°N, remained virtually unchanged. The grazing coefficients were 0.21 and 0.23 day-- 1 on the two experimental days and 0.34 d a y t at 4 5 ° N This level of grazing activity represents 20% removal of the standing stock of Chl a/day or

The western North Atlantic Bloom Experiment

293

6 5 • 8"

4

i"

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3 2 1

0 -- ~--~ 0 2

40N

o~O~o~

, "~ 45N [

I

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14

Nitrate (mmol m ~3) Fig. 8. Silicate versus nitrate plots from the two time-series stations: data from the upper 100 m. Dashed lines arc linear least-squares fits. 50% of the primary production per day at the southern station and 24 and 88% at the northern station, respectively. If a linear grazing response is assumed (see GALLEGOS, 1989), the phytoplankton growth rates ranged with 0.4 to 0.7 doublings day -1, consistent with independent estimates for the ultraphytoplankton growth made during the same study (LI et al., 1993). Mesozooplankton carbon biomass levels were similar at both time-series stations with maxima observed in the u p p e r 100 m; day/night variations were prominent (Fig. 13). Shallow water maxima were evident during the day and night at 45°N, but only at night at 40°N. Mesozooplankton at the more northerly station were dominated by the boreal Calanus finmarchicus, whereas warm water, oceanic species such as Euchirella sp. were more c o m m o n at 40°N. Metabolic measurements suggested that mesozooplankton grazing was an insignificant loss term for phytoplankton at both stations, representing < 10% of the primary production (Table 2). Mesozooplankton N H 4 excretion could have met only a small fraction (2-5%) of the N H 4 requirement of the primary producers. Particulate carbon export at 150 m (sediment traps) represented - 2 4 % of the primary production at 40°N and - 1 4 % at 45°N (Table 3). Fecal pellets represented a significant fraction of this flux at the 45°N station (Table 2). " N e w " production in the upper 50 m based on lSN uptake m e a s u r e m e n t s was approximately two times greater than the 150 m sediment trap N flux but were similar when sediment trap fluxes were extrapolated to the depth of the photic zone, - 5 0 m (Table 3). Decreases in near surface NO3 concentrations over time also were used to estimate new production (Figs 4 and 5); net changes were undetectable at 40°N, but N O 3 disappearance at 45°N was comparable to the 15NO3 uptake estimates (Table 3). DISCUSSION

The spring bloom Phytoplankton biomass and productivity levels and near surface nutrient distributions suggested that the spring bloom was well underway at both time-series stations. The

HARRISON et al.

w.G.

294

50] 4O

Diatoms

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a Fig. 9.

HPLC pigment analyses from the two time-series stations and the southernmos! transect station (32°N),

Table 3.

Export fluxes (mmolin z da5 t)

Sediment trap (150 m)

Pnew (15N) f(0-50 m)

dNO3/dt f(0-50 m)

Trap C-Flux (% Prim. Prod. )

/:ratio (I~N)

45°N Carbon Nitrogen Diel migrant N-flux

13.3 2. I 0,21

-5.b;

26%* (5(/m) 14')o (15(I m)

(I.32

4.6

4(I°N Carbon Nitrogen Diel migrant N-flux

21.6 2,5 0.26

n.d.

38%* (50 m) 24% ( 15(I m)

!~ 3~

4.5

*Extrapolated value using normalized power function n.d. = Not determined.

(MARTINet al., 1987).

295

The western North Atlantic Bloom Experiment

Phytoplankton (mgCm3)

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Fig. 10. Vertical profiles of the major phytoplankton groups identified by light microscopy at the two time-series stations, expressed as carbon biomass; chlorophytes ( C H L O R O ) . cryptophytes ( C R Y P T O ) , prymnesiophytes ( P R Y M N E S ) , diatoms ( D I A T ) and dinoflagellates (DINO).

limited experimental work at these stations ( - 1 week) was not sufficient to construct a clear picture of the temporal stage of the bloom at the time of sampling. Moreover, largescale advection as evidenced by salinity anomaly analysis complicated interpretation of temporal evolution of water masses for the particular geographic regions of the time-series stations. Recent studies in the eastern and western North Atlantic, however, have provided a reasonably good picture of the latitudinal and temporal patterns of spring bloom development (SxRASS and WOODS, 11988; SIEGELet al., 1990; F~ZEL and BERBERIa~, 1990), showing a poleward migration beginning in early spring (February/March) in the southern latitudes and late summer (July/August) at high latitudes. Based on historical CZCS data, maximum spring bloom development at our study site should have occurred during the March-May period, the timing being somewhat earlier at the 40°N than at 45°N (Fig. 14). Bloom development at the major study site in the eastern Atlantic (47°N) should be later (June) based on the satellite color data although the 1989 experimental data did not show this apparent time lag (SCOR, 1990c), suggesting that bloom progression at similar latitudes in the eastern and western Atlantic appeared to be comparable. Biomass partitioning Particulate organic carbon partitioning based on the plankton groupings discussed in this paper (see Table 1) revealed that the major component in the upper 100 m was apparently non-living (i.e. detritus: - 6 0 % ) at both time-series stations, with the balance equally divided between planktonic heterotrophs (bacteria, micro and mesozooplankton) and autotrophs (pico, nano and microphytoplankton; Fig. 15). Of the living component, similar proportions of zooplankton ( - 1 0 % ) and bacteria (-30-40%) were found at the two time-series stations. They differed, however, with respect to the phytoplankton size groups; the ultraphytoplankton (<10 urn) dominated at 40°N and the larger phytoplankton (>10/~m) were more important at 45°N. Because potentially important corn-

296

w.G. HARRISONet at.

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Vertical

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samplings

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at the

two time-series

Chl

a and

stations;

primary

% retained

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rcpeatcd

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ponents of the microzooplankton were not considered in this analysis (i.e. the heterotrophic dinoflagellates and microzooplankton in the -50-200/zm size range), the relative contributions of heterotrophs to the living biomass and living biomass to the total particulates were probably underestimated. Phytoplankton

Contrary to the traditional characterization of the spring bloom dominated by large phytoplankton, principally diatoms (ROBINSON, 1970; PARSONS and LALLI, 1988), the nanoplankton and picoplankton were important components of the phytoplankton assemblages at both time-series stations; at 40°N the ultraphytoplankton, particularly the nanoplankton, accounted for virtually all of the phytoplankton biomass (LI et al., 1992.

The western North Atlantic Bloom Experiment Ultraplankton (mgC m-3)

Ultraplankton (mgC m 3 ) 10 20 30 40 50 60 70 80 0 0L ~1 I I. I I I I~ I VSRF

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4

6

8

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T | N T ~ . i "" 50

50 ~

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150

150

_~ ~ ) l

OLIGO ." H N A N

200 200 Fig. 12. Vertical profiles of ultraplankton (top panels) and microzooplankton (lower panels) at the two time-series stations, expressed as carbon biomass. Ultraplankton comprised of heterotrophic bacteria (BACT) and autotrophs, including "very small red-fluorescing cells" (VSRF), cyanobacteria (CYANO) and photosynthetic nanoplankton (PNAN). Microzooplankton comprised of heterotrophic nanoflagellates (HNAN), tintinnids (TINT) and oligotrichous ciliates (OLIGO).

1993) and most of the p r i m a r y productivity. Half or m o r e of the biomass and productivity were attributable to these small forms at the m o r e northerly station (45°N), with the balance attributable principally to diatoms, dinoflagellates, p r y m n e s i o p h y t e s and cryptophytes. O f these larger p h y t o p l a n k t o n , dinoflagellates a c c o u n t e d for most of the estimated c a r b o n biomass ( 7 0 - 8 0 % ) at b o t h time-series stations. T h e d o m i n a n c e of dinoflagellates was u n e x p e c t e d at 45°N since o t h e r lines of evidence pointed to the strong influence of diatoms (i.e. the depletion of silicate in surface waters, prevalence of fucoxanthin in

w.G. HARRISONet al.

298 Mesozooplankton o

+--

0.2

0.4

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(mgC m'3) 08

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Fig. 13. Vertical profiles o! mesozooplankton at the two time-series stations, sorted by siz,_': ft.2-1.0 mm (upper panels), >1.0 mm (lower panels) and expressed as carbon biomass Open circles/dashed lines = daylight tows: closed circles/solid lines = night tows.

pigment analyses); surface silicate depletion also was noted in the eastern N A B E study (J. MARRA, personal communication). This apparent inconsistency could be explained if many or most of the dinoflageilates were heterotrophic rather than photoautotrophic. From our preserved samples, it was not possible to distinguish between autotrophic and heterotrophic dinoflagellates with light microscopy. The major genera present at both stations were Ceratium, Dinophysis, Prorocentrum, Gymnodinium, Gyrodinium, Oxytoxum, Polykrikos, Protoperidinium and Zygabikodinium. Many species of these genera are known to be heterotrophs or facultative heterotrophs (LESSARD, 1984; GAINES and ELBRACHTER, 1987). Most species of Gymnodinium, Gyrodinium, Oxytoxum and Protoperidinium were <20/~m in diameter and were distributed throughout the water column. Some larger athecate species had diatoms, other dinoflagellates and unrecognizable inclusions in their food vacuoles. We conclude that a significant proportion of this

299

The western North Atlantic Bloom Experiment I

4

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60N 20W 3-

CZCS Pigments (Monthly Means, 1979-86 4

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2

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1

3

4

1

1

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1

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7

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Month

Fig. 14. Temporal variations in near surface pigment concentrations for eastern and western N A B E study sites derived from CZCS ocean color data. Monthly mean values (1979-1986) for 1° squares based on analysis of grey-scale (GS) data and derived from the relationship: Pigment concentration l0 (GS-I1~ 51/83 3 =

community was heterotrophic and that diatoms, indeed, played a more important role in the autotrophic metabolism at 45°N than apparent from estimates of phytoplankton carbon biomass. HPLC pigment analysis also supported this view; peridinin, a major carotenoid pigment of photosynthetic dinoflagellates was present in relatively small proportions at the two time-series stations, but particularly so at 45°N.

300

w.G.

HARRISON et al. 45N

45N

E

4%

MESOZ MICROZ PHYTO>10 PHYTO< II1 BAUF

AUTO ~ 0 DETRITUS

40 N

40N

3%

/

/

\

\,

Total

Particulates

Living

Biomass

Fig. 15. Partitioning of particulate carbon into detrital and living (planktonic) components for the two time-series stations, Values (g C m -'~) and percentages based on m e a n water column integrated values (0-100 m). See Table 1 for computational details and definitions.

Bacteria

The spring phytoplankton bloom supported a significant bacterial biomass and activity at both time-series stations. In the upper 100 m, bacterial production was 12-39% of the primary production. If we assume bacterial growth efficiency to be 50% (COLE eta[.. 1988), then there was an implied bacterial carbon demand (production + respiration) of 24-78% of the primary production, with the higher values found at the more northerly site. Li et al. (1993) have noted that these levels of bacterial demand are equal to or higher than previously published values. Bacterial biomass, although large, did not dominate the phytoplankton in the euphoric zone (<50 m) but did exceed phytoplankton biomass below that depth. For that reason, bacterial activity (i.e. nutrient regeneration) may have contributed to the unexpectedly high NH4 concentrations seen below the Chl a maximum layer at both time-series stations (Fig. 7). A similar but much more pronounced subsurface N H 4 maximum was observed at the 47°N, 20°W site (C. GARSIDE, personal communication). Micro- and mesozooplankton

Microzooplankton represented the largest sink for primary production at both timeseries stations with grazing losses equivalent to 50-88%/day, the largest fraction occurring at the more northerly station. This is certainly consistent with the emerging view that

The western North Atlantic Bloom Experiment

301

microzooplankton, particularly the protozoa, play a major role in the cycling of carbon and other nutrients in the surface ocean (e.g. REID et al., 1991). Because the abundance of the microzooplankton decreased with depth to a lesser degree than did the phytoplankton (as in the case of the bacteria), it is likely that microzooplankton nitrogen excretion also contributed to the development of the subsurface NH4 maximum observed at both time-series stations as discussed previously. One outstanding question remaining relates to the specific contribution of heterotrophic dinoftagellates to the microzooplankton standing stock, their metabolic activity and role in carbon cycling during the bloom. Future studies should focus on those aspects of dinoflagellate biology. Mesozooplankton metabolic activity (grazing, NH4 excretion) had an insignificant impact on primary productivity at either of the time-series stations. Grazing losses represented <10% of the daily production, a figure similar to that found at the JGOFS 20°W site (MORALESet al., 1991) and of the same magnitude found during the spring bloom in other north temperate latitude studies (e.g. D A ~ et al., 1982; BAARS and FRANSZ, 1984). As was the case for grazing, mesozooplankton NH 4 excretion contributed little (<5%) to the phytoplankton demands at the time-series stations as has been found in other spring bloom studies (e.g. DAcc etal., 1982; BAMSTEDT,1985). If, on an annual time scale, mesozooplankton are more important grazers and nutrient recyclers than our results suggest, then phytoplankton and mesozooplankton production cycles in the North Atlantic are not well "phased" during the spring bloom, as PARSONS and LALLI (1988) previously pointed out. The extensive continuous plankton recorder (CPR) data for the North Atlantic also support this view (COLEBROOK, 1979). Temporal mismatch in producer-consumer cycles was apparently not a consideration with regard to the microzooplankton (see above). Fecal pellet production at the 40°N station contributed - 10% to the particulate organic C and N flux to sediment traps, consistent with mesozooplankton grazing of primary producers. At the 45°N station, however, pellets accounted for virtually all of the trap flux, suggesting that carbon and nitrogen sources other than phytoplankton constituted a major portion of the mesozooplankton diet. High fecal pellet contributions to sedimenting organic matter despite low grazing impact on primary producers is not an uncommon occurrence in subtropical oligotrophic waters (e.g. SMALLet al., 1983, 1987), but has been less commonly observed during spring bloom conditions at temperate latitudes (BATHMANNet al., 1987; SMETACEK,1980). Export fluxes

Particulate organic carbon export at the base of the euphotic zone represented 26-38% of the daily primary productivity at the time-series stations, the higher value associated with the more southerly station (40°N). Particulate organic nitrogen fluxes from sediment traps (150 m) were lower by a factor of two than "new" production estimates based on 15NO3 tracer experiments and NO 3 disappearance in the euphotic zone but, as in the case of carbon, were comparable when extrapolated using the formulation of MARTIN et al. (1987) to the same depth horizon. 15N-based f-ratios were similar at the two stations (0.32-0.33) and consistent with f-ratios based on carbon fluxes (sediment trap flux/ primary productivity). BUESSELERet al. (in press) derived f-ratios of the same magnitude (0.29-0.46) from 234Th:238Udisequilibria estimates at approximately the same time (24 April-30 May) at the JGOFS 20°W site (47°N). Model investigations of the seasonal plankton production cycle have yielded similar f-ratios for the spring growth period

302

W . G . HARRISONet al.

@ratio: ~0.20-4).40; FASHAMetal., 1990; see also YENTSCH, 1990). An additional nitrogen export term, associated with mesozooplankton diel migration, which has been found to bc significant in some ocean regions (LONGHURSTand HARRISON,1988), was small (i. e. -,~10'~,; of sediment trap fluxes) during the western NABE (Table 3).

SUMMARY

The spring bloom in the western North Atlantic was well-developed during the Canadian NABE investigation. 20 April-18 May 1989. Processes studies concentrated on two sites (40°N, 47°N: 45°N. 41°W) along an extended N-S transect (32-47°N) where bloom development was maximum. The two time-series sites were similar with regard to various biological properties including: bulk Chl a. primary productivity, zooplankton biomass and activity and the general vertical structure of the plankton communities (bacteria, phytoplankton and zooplankton). Dinoflagellates dominated the biomass of the netplankton at both sites but may have been largely heterotrophs. The time-series sites differed markedlv, however, in other properties (c.g. water chemistry, plankton community size structure and composition). Surface silicate depletion was evident at 45°N but not at 40°N, consistent with the relatively greater importance of diatoms at the more northerly site. Ultraphytoplankton (< 10~m) were dominant at 40°N, accounting for virtually all of the Chl a biomass: at 45°N the ultraphytoplankton comprised ~50% of the biomass. Bacterial biomass and production were important at both sites, bu~ most significant at 45°N where bacteria comprised ~30% of the total plankton biomass0 and bacterial production and respiration demand on primary productivity exceeded 75%. Microzooplankton grazing dominated phytoplankton losses (50-88% of the daily primar) production). Despite their small impact on phyt0plankton losses (via grazing), mesozooplankton fecal matter comprised the bulk of the organic carbon (and nitrogen) matter caught in sediment traps at 45°N. but not at the more southerly station. Export fluxes a~ measured by sediment traps accounted for 25-30% of the daily primary production. Mare of the general hydrographic, chemical and biological features described here were also observed in the eastern Atlantic study (20°W). Acknowledgements--The authors thank Jeff Arming, Carla Caverhilt. Paul Dickic, Leslie Harris, Mark Hodgson, Cheryl LeDrew and AI MacDonald for expert technical assistance and Richard Outerbridge l t~ analysis of CZCS data. Dr Cynthia McKenzie helped in phytoplankton taxonomy.

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