JOURNAL OF GEOPHYSICAL RESEARCH, VOL. 100, NO. C4, PAGES 6665-6675, APRIL 15, 1995

Grazing by microzooplankton and mesozooplankton in the high-latitude North Atlantic Ocean' Spring versus summer dynamics

Dian J. Gifford

Graduate School of Oceanography, University of Rhode Island, Narragansett

Lynne M. Fessenden College of Oceanic and Atmospheric Sciences, Oregon State University, Corvallis

Peter R. Garrahan and Elena Martin Graduate School of Oceanography, University of Rhode Island, Narragansett

Abstract. Grazing on chlorophyll by microzooplankton (<200 •um) and copepods was measured in the mixed layer of the high-latitude North Atlantic Ocean during May and August 1991. No significant grazing by microzøoplankton occurred in May during a spring bloom dominated by colonial Phaeocystis pouchettii and Nitz- schia spp. As the bloom declined, the size distribution of chlorophyll shifted from dominance by the > 20 •um chlorophyll fraction to dominance by the <20 chlorophyll fraction. The impact of grazing by microzooplankton increased as the bloom declined, with microzooplankton consuming 100% of potential daily chloro- phyll production following the bloom. In August,.when the phytoplankton was dominated by the <20 #m chlorophyll fraction, m•cr0zooplankton consumed 37-53% (mean = 41%_+11% s.d.)'of potential daily chlorophyll production. Averaged over all experiments, microzooplankton grazing accounted for 81% of daily chlorophyll production. The grazing impact of Calanus finmarchicus stages C4 and C5, which dominated mesozooplankton biomass in the upper euphotic zone in both spring and late summer, was concentrated on chlorophyll > 20/tin in both seasons; C. f in mar c h ic u s did not consume significant amounts of chlorophyll < 20 •um in either season. Compared to the microzooplankton, copepods did not consume a significant fraction of total chlorophyll in either season, accounting for only -1% of daily chlorophyll production.

Introduction

The objective of this study was to evaluate losses of chlorophyll due to grazing by microzooplankton and mesozooplankton in the mixed layer of the high-latitude North Atlantic Ocean under contrast- ing biological and hydrographic conditions during spring and summer. The research was conducted on RV Endeavor cruises EN224-3 and EN227 in spring and late summer 1991 under the aegis of the Marine Light Mixed Layers (MLML) Accelerated Research Initiative, a multidisciplinary effort fo- cused on the biological, physical and optical dynam- ics of the mixed lay_cr. The MLML study site was occupied t'or 8 days •n May 1991 and 9 days in Aug- ust/Scptcmber 1991.

The MLML study site is located in the North Atlantic Ocean at 59øN, 21øW, south of the Subarc-

Copyright 1995 by the American Geophysical Union

Paper number 94JC00983 0148-0277!95!94JC-00983505.00

tic Front, an area characterized by extreme seasonal forcing of biology and hydrography. Convective cooling of the water column during winter produces adccp mixed layer of at least several hundred meters, which provides new nutrients to the system [Robinson et al., 1979; Plueddemann et al., this issue]. Irradiance and phytoplankton standing stocks are low during winter when phytoplankton growth is believed to be very low. With the onset of stratification, typically in April, standing stocks of chlorophyll increase IWil!iams and Hopkins, 1974; Plueddemann et al., this issue; Stramska et al., this issue], and a strong diatom bloom

reaching 2-5/•g L '•. Calanus finmarchicus and other copepod species appear in the euphotic zone at this time, but their grazing appears to have little impact on the bloom [Dam et al., 1993; Morales et al., 1991; Weeks et al., 1993]. Transition to the summer phytoplankton community, characterized by dinoflag½llates and Rhizosolenia spp., usually occurs in June, when euphausiids, siphonophores and ctcnophores also appear [e.g., Colebrook, 1984; Williams and Lindley, 1982]. Maximum

6665

6666 GIFFORD ET AL.: MICROZOOPLANKTON GRAZING

water column stability occurs in August, and stratifi- cation declines with the onset of deep mixing in September-October.

Nanoplankton and microplankton are defined on the basis of size as organisms 2-20 #m and 20-200 /tin, respectively [Sieburth et al., 1978]. For clarity, we refer to heterotrophs <200/tin as micro- zooplankton. This operational category contains a diversity of protistan taxa including heterotrophic flagellates, dinoflagellat½s, ciliates, and sarcodines as well as metazoan nauplii [Beers, 1978]. Numeri- ,.

cally' heterotrophic flagellates , dinoflag½llates and aloricate ciliates are the most abundant microzoo- plankton organisms and are ubiquitous in the euphotic zones of marine waters. M½sozooplankton are organisms 200-2000 #m, and consist predomi- nanfly of crustacean zooplankton.

It is now recognized that the microzooplankton are major consumers of phytoplankton in the sea [e.g., Banse, 1992 and references therein], exerting a greater grazing impact than herbivorous mesozoo- plankton [e.g., Smetacek 1981; Paranjape et al., 1985]. Banse [1992] argued that on a timescale of days the instantaneous grazing 'rate of zooplankton, in toto, is greater than the instantaneous rates of vertical advection and mixing by at least an order of magnitude, and is the same order of magnitude as the instantaneous rate of phytoplankton cell divi- sion. Hence, grazing is a critically important loss term in phytoplankton dynamics. Because micro- zooplankton are the major grazers in pelagic food webs, their grazing activities exert an important impact on phytoplankton losses in the sea. Al- though its importance is recognized, microzooplank- ton grazing dynamics have not been studied exten- sively in oceanic areas. An objective of this study is to add to our knowledge of oceanic grazing process- es, particularly in the context of contrasting hydro- graphic conditions during changing seasons.

Methods

Microzooplankton Grazing

Microzooplankton grazing in the mixed layer was measured by the seawater dilution technique [Lan- dry and Hassett, 1982; Landry, 1993], a simulated in situ method. Of the several methods available for this purpose, the dilution technique is simple in concept and has proven robust to potential viola- tions of its underlying assumptions [ Gifford, 1988; Gallegos, 1989]. The method involves diluting seawater containing the in situ protist (=phyto- plankton + protozoa) assemblage with filtered seawater from the Same source. A series of dilution treatments is set up, creating a gradient of grazer abundance. The phytoplankton assemblage in each treatment, freed from predation by micrograzers, grows at a rate which is a linear function of grazer density [Landry, 1993].

The change in •phytoplankton concentration with time is calculated by

Pt •- Po ½Cu'•)t (1)

or

lit In (Pt-Po) = /t-g (2)

where Pt and Po are phytoplankton concentrations at the beginning and end of the experiment, # is the instantaneous rate of phytoplankton growth, and g is the instantaneous rate of phytoplankton mortality due to grazing. The term on the left side of equa- tion (2) is the "apparent phytoplankton growth rate •. The y intercept of the line is the instantaneous rate of phytoplankton growth in the absence of grazing. The negative slope of the line is the instantaneous rate of phytoplankton mortality due to grazing. Values of # and g were calculated from changes in chlorophyll a, plotted as a function of grazer dilu- tion following incubation of the dilution treatments [Landry, 1993]. Grazer dilution was expressed as the time-averaged densities of aloricate ciliates because these organisms dominated the heterotro- phic protists •20 /tm in our experiments, and appropriate data from microscopic counts were available for them. Changes in chlorophyll a were also plotted as a function of chlorophyll dilution, according to Landry and Hassett's [1982] original formulation of the method. The results (not shown) did not differ significantly from those plotted as a function of grazer dilution. The data were analyzed by linear regression, and tests of significance were done according to Sokal and Rohlf [1981]. Initial standing stock of phytoplankton consumed and po- tential phytoplankton consumed were calculated according to Gifford [1988], where potential chlorophyll production Pp is

Pp = ( Po ek ) ' Po (2})

actual chlorophyll production Pa is

Pa = (Po e(t's)) - Po (4) and potential chlorophyll production consumed is

Pp' Pa- (5)

Bulk seawater was collected from the mixed layer using acid-cleaned Go-flo bottles equipped with silicone o-rings. The seawater was diluted with filtered seawater from the same source by factors of 0% to 95%. The number of treatments in a given experiment depended on the amount of seawater available from Go-flo casts. The 100% dilutions (i.e., filtered seawater) were incubated as controls for phytoplankton growth in the filtered seawater [Li, 1990]. Because no significant growth of chloro- phyll occurred in these treatments, the data were not corrected and the controls are not discussed further. Three replicates of each treatment were incubated in I-L polycarbonate bottles for 24-48 hours in an on-deck rotating-wheel incubator whose temperature was maintained by flowing seawater. Bottles were covered with neutral density mesh to simulate in situ light conditions. Samples for total chlorophyll, chlorophyll •20 #m, and major phyto-

GIFFORD ET AL.: MICROZOOPLANKTON GRAZING 6667

plankton nutrients were collected from all bottles at the beginning and end of each experiment. Chloro- phyll samples wcrc collected in triplicate on GF/F filters (Whatman International, Ltd., Maidstone, England, nominal pore size 0.7 •tm) and stored in liquid nitrogen until analysis. Filters were extracted in cold 90% acetone in the dark for 48 hours, then analyzed by fluoromctry [Parsons et al., 1984]. Samples for microplankton, used to determine grazer dilution, wcrc collected from one replicate bottle of each dilution treatment at the beginning and end of each experiment and preserved with 10% (vol/vol) acid Lugol's solution [Throndsen, 1978]. They wcrc concentrated by settling and then trans- fcrred to an inverted microscope counting chamber. Microplankton wcrc identified and enumerated

using a Zeiss Axiovert inverted microscope at 200X magnification. A total of 100 mL of seawater was processed from each experimental and control bottle. In most experiments, a minimum of 200 microplanktcrs was enumerated [Venrick, 1978]. Samples for nutrient analyses wcrc frozen immedi- ately after collection, then analyzed by our MLML colleague B. Jones using the methods of Sakomota et al. [1990].

Six experiments were performed in May and August 1991 (Table 1). The first experiment was done on May 16 during a bloom dominated by colonial Phaeocystis pouchettii and Nitzschia spp. when the mixed layer was -•40 m deep. The second experiment was done on May 18 when the bloom was declining, as evidenced by declining "C assimilation rates [Marra, et al., this issue]. On May 20-21, a strong storm with peak winds of ap- proximately 22 m s '• [Plueddemann et al., this issue] mixed the water column to > 300 m, diluting chlorophyll by a factor of 3.5 and dissipating the remainder of the bloom. The third experiment was performed on May 22, following the storm, when the mixed layer had restratified. The three August

experiments were performed under stratified condi- tions, when mixed layer depth was -20-40 m.

Mtsozooplankton Grazing

Six experiments were done during spring and late summer following methods described by Gifford [1993] (Table 2). The experimental design utilized two treatments: an experimental treatment consist- ing of bulk seawater from the middle of the mixed layer incubated in bottles with copepods and a control treatment in which bottles contained only bulk seawater. Copepods wcrc collected at night by vertical hauls of a 335/tm mesh, 1-m diameter clos- ing ring net. Calanus finmarchicus were sorted to stage under a dissecting microscope using a wide- bore pipette. The copepods wcrc acclimatcd to the experimental conditions for 24 hours by transferring them to 1-L polycarbonate bottles containing seawa- ter collected from the mixed layer and placing the bottles in a darkened, water-cooled, on-deck incuba- tor equipped with a rotating wheel. Immediately before setting up the experimental treatments, seawater was collected from the middle of the mixed layer, as described above for the microzoo- plankton grazing experiments. Acclimatcd copepods were transferred to 1-L polycarbonate incubation bottles, the bottles wcrc topped up with seawater, sealed with parafilm to exclude air space, and wrapped with neutral density screening. They were then rotated slowly end over end in the on-deck incubator for 1-2 hours before initial samples for total chlorophyll and chlorophyll < 20/tm were coil- cctcd. The remainder of the bottles wcrc incubated for 24 hours. Upon termination of each experiment, samples for total chlorophyll and chlorophyll <20 /tm wcrc collected from all bottles. Chlorophyll was analyzed by fluorometry as described for the micro- zooplankton grazing experiments. Per capita clear- ance rates on chlorophyll wcrc calculated according to Frost, [1972].

Table 1. Initial Conditions of Microzooplankton Grazing Experiments

Date in Chlorophyll, 1991

May 16 2,89

May 22 0.59

August 24 2.27

August 27 1.80

August 30 1.19

i i i , , i ,

Depth of Mixed Water Incubation Layer

Collection, Light, Temperature, Time, Depth, (m) (%) (øC) (hours) (m)

20 25 8.40 24 40

20 50 8.36 48 20

15 25 12.86 48 20

5 50 12.26 48 40

10 75 11.81 48 40

Temperature is at depth of water collection. Light is percent of surface illumination in flow-through incubators.

6668 GIFFORD ET AL.: MICROZOOPLANKTON GRAZING

Table 2. Initial Conditions of Calanus finmarchicus Grazing Experiments

Chlorophyll, Date in 1991 (fg L 'l)

May 17 1.57

May 20 0.90

May 25 1.51

August 29 1.39

August 31 1.45

September 1 1.40

Incubation Copepods, Time, (number/ Copepod (hours) bottle) Stage

24.50 10 C4

25.25 10 C5

24.00 10 C4

27.08 15 C5

27.08 13 C5

25.00 15 C5

Temperature is at depth of water collection.

Depth of Water

Collection, (m)

Temperature, (øc)

10 8.43

10 8.32

5 9.02

20 11.81

10 10.88

10 11.48

Results

Chlorophyll

The standing stock of chlorophyll in the mixed layer decreased during May from 2.89 gig L '; on May 16 during the Phaeocystis bloom to 0.59 fg L '• on May 22 following the storm which dispersed the bloom. By May 25, chlorophyll concentration had increased to 1.51 fg L '• following 2 days of bright sunshine. Chlorophyll also decreased during late summer, from 2.27 fig L '• on August 24 to 1.40 fig L '• on September 1 (Tables 1 and 2). Chlorophyll size fractions in the microzooplankton and copepod grazing experiments are given in Table 3. On May 16, during the Phaeocystis bloom, 56% of the chlorophyll was > 20/•m. As the bloom declined on May 17 and 18, the chlorophyll size distribution shifted and 24% and 40%, respectively, of total chlorophyll was > 20 fm. After the storm dispersed the bloom on May 20, 67-81% of the chlorophyll was located in the <20/•m fraction. During August, nanoplankton dominated, with 67-83% of the chlo- rophyll < 20

Microplankton Assemblage

Phaeocystis pouchettii colonies were not pre- served by the acid Lugol's fixative and were not enumerated in the microplankton samples. Of the phytoplankton which were preserved, Nitzschia spp. dominated the phytoplankton > 20 fm numeri- cally in May. Centtic diatoms and thecate dino- flagellates were also present at lower levels. Nu- merical abundances of both microzooplankton and microphytoplankton decreased following the May 20 storm. In August, the phytoplankton assemblage was more diverse, consisting of Rhizosolenia spp. and a number of thecate and athecate dinoflag- ellat½s (Table 4). Aloricate ciliates dominated the

microzooplankton during both May and August. Ciliates < 10/•m dominated in May. In August, cil- iate cell size was larger, with cells >20/•m domi- nant. Heterotrophic dinoflagellates, including the genera Protoperidinium and Gyrodinium were present during both seasons, and small (< 10 dinoflagellates of unknown trophic status were

Table 3. Chlorophyll Size Fractions in Microzooplankton and Mesozooplankton Grazing Experiments

Date in 1991

May 16

May 17

May 18

May 20

May 22

August 24

August 27

August 29

August 30

August 31

September 1

Proportion of Chlorophyll in Size Fraction

ii , !

>20 fm <20 fm

0.56 0.44

0.24 0.76

0.40 0.60

0.33 0.67

0.19 0.81

0.25 0.75

0.31 0.69

0.17 0.83

0.33 0.67

0.24 0.76

0.21 0.79 II III

GIFFORD ET AL.- MICROZOOPLANKTON GRAZING 6669

Table 4. Abundances (Number L '1) of Major Taxa in Microplankton Assemblages in Microzooplankton Grazing Experiments.

Date Aloricate Tintinnid in 1991 Ciliates Ciliates

May 16 3303 66

May 18 4246 176

May 22 2814 22

August 24 5775 109

August 27 6721 175

August 30 7145 220

Protoper- Cerat- Rhizo- idinium Gyrodin- Centric ium solenia spp. iu m spp. Diatoms spp. spp.

330 1233 6781

242 418 4312

242 220 1275

219 1400 --- 438 930

307 1030 --- 307 1666

154 989 --- 330 1099 I II I I

abundant in August/September. Heterotrophic flagellates <20/tin were present (C.A. Knudsen, unpublished data, 1993), but were not enumerated in the samples preserved with acid Lugo!'s solution. Numerical abundances of heterotrophic protists were approximately twice as high in Aug- ust/September as in May (Table 4). Nutrients

Initiel silicate concentrations increased from

/tg-at L 4 on May 16 to 3.79 •ug-at L '• on May 22 and

from 0.47 •ug-at L '1 on August 24 to 1.26 fig-at L '• on August 30. Phosphate concentrations averaged 0.55 •ug-at L '• in the three May experiments and increas- ed in August from 0.07 fig-at L '• on August 24 to 0.18 •ug-at L '1 on August 30. Nitrate concentration was 10.49 •ug-at L '• on May 16 during the Phaeo- cystis bloom, decreased to 9.40/zg-a.t L '• on May 18, and increased to 10.87 fig-at L" on May 22 after the storm. Nutrient concentrations in the incubation bottles did not change appreciably during the microzooplankton grazing experiments (data not

1.00

16 May 1991

Total chlorophyll

0.50 -

.

0.00 -

- ß

-0.50 -

-

-I.OO

o.o

I.OO

0.5o

-o.5o ß

-I.00 0.0 0.25

18 May 1991

Total chlorophyll

' t

1.0

0.5'

22May 1991

Total chlorophyll

I I ,I I I I I I I

0.25 0.5 0.75 I.O O.O 0.25 0.5 0.75 I.O O.0 025 0.5 0.75

Chlorophyll < 20 pm

I.OC

"0.50

_inn

Chlorophyll <20 ,am

1.00

0.50

1.0 0.0

Chlorophyll <20 pm

I I i I

0.5 0.75 0.25 0.5 0.75 1.0 0.0 0.25 0.5 0.7 5

Fraction undiluted seawater

Figure 1. Dilution curves for microzooplankton grazing during May, 1991.

1.0

1.0

6670 GIFFORD ET AL' MICROZOOPLANKTON GRAZING

1.00

075

0.50

• o.a5

0.00

0.0

1.00

0.75

050

O.25

0.00

0.0

24 August 1991

Total chlorophyll

ß

ß ß

27 August 1991

Total chlorophyll

I I I , I I

0.25 0.5 0.75 1.0 0.0 0.25 0.5 0.75 1.0

1.00

0.75

0.50

0.25

0.00

0.0

oo

ß ß

ß

I

Chlorophyll < 20 ,urn Chlorophyll < 20 pm

1.00

).75

)50

3.25

).oo

o.o

t ß

ß

I I I I I I

0.5 0.75 1.0 0.25 0.5 0.75 1.0 0.25

.00

L75 -

-

50

.25 -

.

.00,

0.0

30 August 1991

' Total chlorophyll

I I I

0.25 0.5 0.75 1.0

Chlorophyll <20 ,um

I I

0.5 0.7 5 1.0

Fraction undiluted seawater

Figure 2. Dilution curves for microzooplankton grazing during August, 1991.

shown), indicating that grazing estimates were not biased by nutrient limitation, a possibility that is of concern in experiments utilizing the seawater dilution technique [Landry and Hassett, 1982].

Microzooplankton Grazing

The fraction of potential daily chlorophyll produc- tion consumed varied among experiments and between chlorophyll size fractions. Grazing curves from the dilution experiments are given in Figures 1 and 2, and results are summarized in Table 5. While total and <20 #m chlorophyll fractions were analyzed, the size fractionation was not perfect due to a number of factors, including cell breakage and clogging of the filter mesh. Consequently, differ- cnccs between total chlorophyll and <20/•m chloro- phyll fractions could not be distinguished unambigu- ously, and it was not possible to quantitatively estimate grazing on chlorophyll >20/tm. Thus, in this study, changes in the <20/•m chlorophyll frac- tion are used to indicate microzooplankton grazing loci when the chlorophyll was dominated by large (> 20 /•m) particles. There was no significant grazing (g not significantly different from zero; p•_O.05) on either total chlorophyll or on the <20 #m fraction in the May 16 experiment during the bloom. Microzooplankton grazing was concentrated on the <20 #m chlorophyll fraction in the experi- ments done during the decline of the bloom (May 18) and after the storm (May 22). In the three August experiments, there was no significant grazing

on chlorophyll <20 #m, despite the fact that this fraction dominated the total chlorophyll. Rather, .grazing was located on the total chlorophyll, indicat- ing that phytoplankton >20 #m were being con- sumed. Phytoplankton growth and microzoo- plankton grazing were out of balance in the May 18 experiment during the decline of the bloom, when grazing exceeded growth, and more than 100% of potential daily chlorophyll production was con- sumed. In the experiment done on May 22 follow- ing the storm, grazing and growth were in approxi- mate balance, and -100% of potential daily chloro- phyll production was consumed. Phytoplankton growth exceeded grazing in the three August experi- ments, when microzooplankton consumed 37-53% (mcan=41%_+11%) of the potential production of total chlorophyll per day. The positive slope of the grazing curve in the <20 •tm chlorophyll fraction on August 30 indicates that something was amiss with the size fractionation for that experiment. Hence, grazing impacts on the <20 •tm chlorophyll fraction were not calculated for that date (Table $).

Mcsozooplankton Grazing

At the MLML site in 1991, C. finmarchicus dominated the mtsozooplankton in the upper water column in spring [Batchelder et al., this issue] and late summer [Cowles and Fessenden, this issue]. There was no copepod mortality in any of the experiments, and copepods cleared 12% + 0.0% s.d. and 21% + 11% s.d. of the chlorophyll on average from the incubation bottles during the May and

GIFFORD ET AL.' MICROZOOPLANKTON GRAZING

Table $. Microzooplankton Grazing Impact in May and August 1991.

Date in 1991 /•, d '• g, d '• r p

Fraction Initial

Chlorophyll Standing Stock

Consumed, d-•

Total Chlorophyll

May 16 -0.13 0.13 0.23 NS NS (0.•8) (0.•3)

May 18 0.02 0.07 0.44 NS NS (0.0S) (0.64)

May 22 0.63 0.70 0.77 NS NS (0.16) (0.49)

August 24 0.30 0.11' 0.58 0.01 0.24 (0.06) (0.04)

August 27 0.45 0.24' 0.82 0.001 0.38 (O.O6) (0.05)

August 30 0.44 0.14' 0.75 0.001 0.16 (O.04) (0.03)

Chlorophyll < 20

May 16 -0.39 -0.19 0.21 NS NS (0.30) (0.22)

May 18 0.13 0.83* 0.84 0.001 1.0 (0.17) (0.15)

May 22 0.87 1.01' 0.95 0.001 0.31 (0.09) (0.11)

August 24 0.27 0.08 0.01 NS NS (0.10) (0.06)

August 27 0.41 0.002 0.01 NS NS (0.11) (0.10)

August 30 0.02 -0.35 NC NC NC (0.11) (0.11)

Here, # is the instantaneous rate of phytoplankton growth, g is the instantaneous rate of microzooplankton grazing, r is the correlation coefficient, p is significance level, NS is not significant, NC is not calculated. Values in parentheses are standard errors.

*g>0; p < 0.05.

Fraction Potential

Chlorophyll Production

Consumed, d-•

NS

> 1.0

> 1.0

0.37

O.53

0.32

NS

> 1.0

> 1.0

NS

NS

NC

6671

August experiments, respectively. Clearance rates of Calanus finmarchicus C4 and C5 on total

chlorophyll in May averaged 1.05 _4- 0.0 s.d. n•L copepod 'a h '•. In August, clearance rates of . finmarchicus C5 ranged from 0.88 to 2.83 mL copepod '• h '• (mean =1.88_+0.98 s.d.). In both seasons, C. finmarchicus cleared chlorophyll <20 /•m at lower rates than they cleared total chlorophyll

(Table 6). Per capita ingestion rates of heterotro- phic protists and chlorophyll were also measured in

•, murc n s the experiments. However, . fin icu diet and feeding physiology at the MLML site are the subject of a separate study [D.J. Gifford and L.M. Fessenden, manuscript in preparation, 1994] and will not be addressed further here.

6672 GIFFORD ET AL.: MICROZOOPLANKTON GRAZING

Table 6. Grazing Rates of Calan us finmarchicus.

Clearance Rate, mL copepod '1 h '1 ß , ,

Date in 1991 Total

Chlorophyll t i i t it t

May 17 1.05 (0.0)

Chlorophyll < 20 •m

i i i, i

0.35

(0.61)

May 20 1.05 0.0 (0.0) (0.0)

May 25 1.05 (0.73)

August 29 1.93 0.70 (0.35) (0.0)

August 31 2.83 0.41 (0.47) (0.47}

September 1 0.88 0.02 (0.67) (0.04)

i , i i i i i i i! i

Values in parentheses arc standard deviation units.

Discussion

Microzooplankton were major grazers of chloro- phyll in the mixed layer at the MLML site during May and August 1991, consuming up to 100% of potential daily production of chlorophyll <20 #m in May after the bloom dispersed and 32-53% of potential daily chlorophyll production in August under stably stratified conditions. The presence of colonial P. pouchettii, the dominant spring bloom organism, may have inhibited microzooplankton grazing [Estep et al., 1990], although this question cannot bc addressed by our data. The bloom was declining prior to the May 19-20 storm, as evidenced by declining •4C assimilation rates [Matra et al., this issue] and decreasing numerical abundances of microphytoplankton (Table 4). In the microzoo- plankton grazing experiments, chlorophyll growth rates were negative during the peak of the bloom, increased to 0.02 d '• (=0.03 doublings d '•) during the decline of the bloom, and increased to 0.63 d" (= 0.91 doublings d '•) following dissipation of the bloom by the May 20 storm. Changing light condi- tions probably contributed to the abrupt increase in phytoplankton growth following the storm: overcast skies prior to and during the storm were followed by 2 days of bright sunshine. The magnitude of micro- zooplankton grazing shifted dramatically as the bloom declined, from no impact to consumption of virtually all of the potential chlorophyll production in the <20/tin fraction. Because the bloom was dispersed shortly after wc arrived on station, the impact of microzooplankton grazing during the

bloom under non-Phaeocystis conditions could not bc investigated in this study. At the MLML site in August, chlorophyll growth rates ranged from 0.30-0.45 d '1 (=0.43-0.65 doublings d't). Micro- zooplankton grazing impact was concentrated on the larger phytoplankton, although -70% of the chloro- phyll standing stock was <20/tin. This result is unexpected; however, microzooplankton grazing studies done in the Gulf of Mexico showed a similar result [Strom and Strom, 1994], perhaps indicating some specificity in feeding interactions within the microzooplankton during the particular experiments.

The microzooplankton grazing rates wc observed arc consistent with rates measured during other studies conducted in the same high-latitude area of the North Atlantic (Table 7). Combining our obser- vations with those of Weeks et al. [1993] and Burkill et al. [1993] suggests a seasonally varying pattern of microzooplankton grazing with little or no impact during the peak of the spring bloom, followed by increased impact as the bloom declines. Our measurements of microzooplankton grazing during summer are virtually identical to those of Burkill et al. [1993]. These impacts are lower in magnitude than those observed at more southerly latitudes in the North Atlantic [Burkill et al., 1993; Verity eta!., 1993; Weeks et al., 1993 I. The clearance rates measured for Calanus finmarch- i cus stages C4 and C5 are similar to those mea- sured using independent methods by Cowles and Fessenden [this issue], and fall well within the range observed by other investigators [reviewed by Cono- ver, 1978]. Applying the observed clearance rates of C. finmarchicus (Table 6) to their numerical abundances in May [Batchelder et al., this issue] and August [Cowles and Fessenden, this issue], C. finmarchicus were capable of clearing on the order of .01 L d '• in May and August/September, i.e., approximately 1% of the mixed layer. This estimate assumes that the mcsozooplankton are dominated by C. finmarchicus, as observed by Batchelder et al. [this issue] and Cowles and Fessenden [this issue] and that the smaller life history stages feed at the same rates as the C4 and C5 studied in the experiments. Because C. fin mar- ch icu s has adiel feeding cycle in this area (T. J. Cowles, unpublished data, 1993), hourly clearance rates were extrapolated to a 12-hour day. By any measure, compared to microzooplankton, copepods were minor grazers of phytoplankton at the MLML site during both May and August, in agreement with independent observations of Cowles and Fessen. den [this issue] and with other studies in adjacent areas of the North Atlantic [Burkill et al., 1993; Dam et al., 1993; Morales et al., 1991; Weeks et al., 1993].

The observed low grazing impacts during the high-latitude spring bloom indicate that processes other than grazing must affect the fate of phyto- plankton production, in accord with observations made during the Joint Global O•ean Flux Study North Atlantic Bloom Experiment [e.g., Lochte et al., 1993]. Our observation, and that of Burkill et

GIFFORD ET AL.: MICROZOOPLANKTON GRAZING 6675

Table 7. Grazing Impact of Microzooplankton and Mesozooplankton in the High-Latitude North Atlantic Ocean.

Primary Production Consumed, % d '•

Location Season Microzooplankton M½sozooplankton Source i i i i i i i

60øN, 20øW Spring 25 <2 Weeks et al. late-bloom [1993]

60øN, 20øW Mid-summer 39 <2 Burkill et al. [1993]

59øN, 21øW Spring 0 Phaeocystis bloom

59øN, 21øW Spring 100 post-bloom

59øN, 21øW Summer 41

1 This study

This study

1 This study

al. [1993], that less than 50% of the phytoplankton production is grazed during summer, is more puz- zling. In August 1991, an unknown fraction of the >20 #m phytoplankton consisted of large Rhizo- solenia cells, which are not expected to be utilized efficiently by the microzooplankton organisms. In concert with the observed low mesozooplankton grazing impact, the fate of at least a portion of the summer phytoplankton assemblage must be either to be consumed by other pelagic herbivores (e.g., gelatinous macrozooplankton) or to sink out of the mixed layer. It is instructive to consider the impact of grazing over timescales greater than the dura- tions of our short-term experiments. Averaging over spring and summer, the ratio of phytoplankton growth to microzooplankton grazing is 0.81. Adding the --1% consumed by mesozooplankton indicates that --82% of the phytoplankton production in the mixed layer of the high-latitude North Atlantic is grazed by the microzooplankton and mesozooplank- ton, leaving the remainder to be grazed by other herbivores or exported.

Acknowlcdgmcnta. The research was supported by the U.S. Office of Naval Research under the aegis of the Marine Light Mixed Layers Accelerated Research Initiative (grant N00014-90-J-1437 to D.J. G.). This support is gratefully acknowledged. We thank the captains and crew of RV Endeavor, and L. Sullivan and I. Bitte of Lamont-Doherty Earth Observatory for logistical support in the field. We are grateful to all of our MLML colleagues, es- pecially chief scientist J: Marta, C: A: Knudsen, M. J. Perry, H. Batchelder, T. Cowles, M. Latz, M. K. Talbot, and J. Sullivan. We thank our Icelandic colleague T. Thordadottir for educating us about North Atlantic phytoplankton and graciously intro- ducing us to her country. Special thanks to B. Jones

for analyzing the nutrient samples from the micro- zooplankton grazing experiments. Critical reviews by D. Stoecker and two anonymous referees greatly improved the manuscript. Contribution number 14 of the Marine Light Mixed Layers program.

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GIFFORD ET AL.: MICROZOOPLANKTON GRAZING 6675

L. M. Fcsscndcn, College of Oceanic and Atmo- spheric Sciences, Oregon State University, Corvallis, OR 97331.

P. R. Garrahan, D. J. Gifford and E. Martin, Graduate School of Oceanography, University of

Rhode Island, Narragansett. R102882-1197. (e-mail: gifford @g sosun 1 .g so.uri.½du )

(Received November 10, 1993; revised March 30, 1994; accepted April 13, 1994.)