Sampei, M, et al. 2021. An estimation of the quantitative impacts of copepod grazing on
an under sea-ice spring phytoplankton bloom in western Baffin Bay, Canadian Arctic.
Elem Sci Anth, 9: 1. DOI: https://doi.org/10.1525/elementa.2019.00092

RESEARCH ARTICLE

An estimation of the quantitative impacts ofcopepod grazing on an under sea-ice spring
phytoplankton bloom in western Baffin Bay,
Canadian Arctic
Makoto Sampei1,2,*, Louis Fortier3,4, Patrick Raimbault5, Kohei Matsuno1,6,
Yoshiyuki Abe7, Bernard Quéguiner5, Augustin Lafond5, Marcel Babin3,4, andToru Hirawake1,6,8
This study aimed to quantify the impact of copepod grazing on the productivity of phytoplankton during an
under sea-ice spring phytoplankton bloom (USPB) in western Baffin Bay. To quantify positive and/or negative
impacts of copepod grazing on primary production and the interaction between copepod grazing andphytoplankton species, we sampled seawater and zooplankton under the landfast sea ice every 2–3 days
between May 24 and July 10, 2016. Samples were analyzed for estimation of primary production,
chlorophyll-a (chl-a) concentration, diatom abundance, and copepod fecal pellet (FP) production/grazing rate.
Analyses of chl-a concentration, primary production, and FP production/grazing rate revealed clear temporalchanges and a mismatch between primary production and copepod consumption.The FP production/grazing rate
reached a maximum (9.4/31.2 mg C m–2 d–1) on June 16 before the USPB phase and suddenly decreased to 0.7/2.4
mg C m–2 d–1 on June 21, despite an increase in primary production to 74.0 mg C m–2 d–1.The copepod grazing rate
(3.7 mg C m–2 d–1) was low relative to primary production (344.6 mg C m–2 d–1) during the USPB phase (after June20). While our estimates illustrate that copepod grazing did not limit the maximum daily primary production
during the USPB, the low grazing pressure (2% of primary production) may have been an additional contributor
to the reduction in total primary productivity at the end of the USPB period due primarily to the low supply ofregenerated nitrogen-containing nutrients to drive regenerated production.

Keywords: Under sea ice, Grazing, Fecal pellets, Copepod, Top-down control, Spring bloom, Arctic water

1. Introduction
In the context of global change, many studies on the fateof primary productivity have been conducted to quantify
the responses of the marine ecosystem and biogeochemical cycling to ongoing alteration of the physical environment, such as sea-ice and glacial ice conditions in Arctic
1

Faculty of Fisheries Sciences, Hokkaido University, Hakodate,
Hokkaido, Japan

2

Fisheries and Oceans Hakodate, Hakodate, Hokkaido, Japan3

Department of Biology, Laval University, Québec, QC, Canada

4

Takuvik Joint International Laboratory, Laval University(Canada) - CNRS (France), Québec, QC, Canada

5

Mediterranean Institute of Oceanography, Marseille, France

6

Arctic Research Center, Hokkaido University, Sapporo,
Hokkaido, Japan

7

Office for Enhancing Institutional Capacity, Hokkaido
University, Sapporo, Hokkaido, Japan

8

National Institute of Polar Research, Tachikawa, Tokyo, Japan* Corresponding author:
Email: m.sampei@marine-hakodate.jp

waters (e.g., Tremblay et al., 2006; Tremblay et al., 2012;
Reigstad et al., 2011). Although the ecological and biogeochemical importance of production by ice algae in Arctic
waters has been identified (e.g., Gosselin et al., 1997; Leeet al., 2008; Gradinger, 2009), most studies on primary
production and its ecological roles in the Arctic seasonalice zone during the most productive season (i.e., spring)
have been conducted in open waters because of the logistical difficulties of working in sea-ice-covered waters. In
recent years, massive large-scale under sea-ice spring phytoplankton blooms (USPB) have been observed in Arctic
waters (e.g., Arrigo et al., 2012, 2014; Spall et al., 2014).
The current estimate of primary production (5–10 g C m–2
yr–1) may represent a drastic underestimate when compared with a scenario that includes the USPB (>70 g C
m–2 yr–1) in Chukchi shelf water (Arrigo et al., 2014).
Primary production is affected by top-down control (i.e.,
controlled by feeders) and bottom-up control (i.e., controlled by nutrient availability and photosynthetically active
radiation in sea-ice-covered waters) in the water column(e.g., Verity and Smetacek, 1996; Wassmann, 1998). Top-Art. 9(1) page 2 of 13

down control can affect the taxonomic structure, biomass,and productivity of the primary producers in the watercolumn, the phytoplankton (Campbell et al., 2009; Sherret al., 2009), while primary production/producers impact
the biomass and taxonomic structure of herbivores such as
copepods in the water column (Springer et al., 1989).
Despite the ecological importance of the USPB in seaice-covered waters under ongoing rapid changes in sea-ice
conditions (e.g., sea-ice coverage, thickness, and timing ofretreat), the relationships between processes that regulate
the USPB (e.g., top-down and bottom-up controls) are

Sampei et al: copepod grazing pressure on the USPB

unclear. This article focuses on the top-down control by
copepod grazing activity during the USPB period as a partof the Green Edge project. We specifically address thequantitative impacts of copepod grazing on the USPB in
southwestern Baffin Bay, Canadian Arctic.
2. Materials and methods
2.1. Study area

Baffin Bay is located between the Canadian Archipelago
and Greenland, bordered by the Labrador Sea and theAtlantic Ocean in the south and connected to the Arctic

Figure 1. Bathymetrical map with location of the sampling site on landfast ice in western Baffin Bay. Red closed circle
shows the sampling site. DOI: https://doi.org/10.1525/elementa.2019.00092.f1

Sampei et al: copepod grazing pressure on the USPB

Ocean by the Nares Strait in the north (Figure 1). The
water originating from the Arctic Ocean and the Atlantic
Ocean flows, respectively, from north to south on thewestern side of Baffin Bay and from south to north on theeastern side (Tang et al., 2004). Our study site (ice camp)
was located on landfast sea ice on the eastern coast of
Baffin Island (67.48 N, 63.79 W, water depth of 350 m)
in southwestern Baffin Bay and was representative of themarine conditions prevailing in western Baffin Bay interms of water masses and sea-ice conditions (see Oziel
et al., 2019, and references therein).
Sea-ice thickness was approximately 1.3 m on March24, 2016 (beginning of the study period), about 1 m on
July 8, 2016 (end of the study period), and ranged from 1
to 1.5 m thick during the study period (Oziel et al., 2019).
Snow cover thickness on the sea ice was approximately 30
cm before snow melt initiation on June 3, 2016, and gradually decreased to 8 and <1 cm until the appearance ofmelts pond on June 17, 2016 (Oziel et al., 2019). Concentration of the nutrients nitrate (NO3–), phosphate (PO43–),and orthosilicic acid (Si(OH)4) within the upper 20 m
before June 16, 2016, were consistently high at >5,>0.8, and >6 mmol L–1, respectively (Oziel et al., 2019).
These nutrient concentrations decreased gradually
between June 16 and July 7, 2016, to <1, <0.6, and <3mmol L–1, respectively (Oziel et al., 2019). The nutrient
profiles suggested that the USPB was slowed by nitrogen
limitation in the water under landfast ice.
2.2. Chlorophyll-a (chl-a) concentration in thewater column

Water sampling with Niskin bottles was conducted ina heated tent set up over a 1  1 m hole on the landfast
ice every 2–3 days between May 24 and July 8, 2016, aspart of the Green Edge 2016 field campaign in western
Baffin Bay. The seawater samples were taken at five
depths: 1.5 (bottom of the sea ice), 5, 10, 20, and 40 m.
To determine chl-a concentration, a subsample of the seawater was filtered through a glass fiber filter (Whatman
GF/F, 0.75 mm pore size). Filtered samples were immediately soaked in 90% acetone to extract pigments underdark and freezing (–20  C) conditions for 24 h (Persons etal., 1984). The fluorescence intensity was measured witha Turner Designs 10AU fluorometer (San Jose, CA) calibrated against a pure chl-a standard (Sigma, St. Louis,MO), and chl-a concentration was calculated according
to the acidification method (Holm-Hansen and Riemann,
1978). The chl-a concentration was integrated between
0 and 40 m and expressed in mg chl-a m–2.
2.3. Primary productivity of under sea-ice
phytoplankton

Rates of C fixation by phytoplankton (primary production)
were measured using a dual 13C/15 N isotopic technique(Raimbault et al., 1999) as described in Massicotte et al.
(2020). Column-integrated primary production between
0 and 20 m was calculated on the basis of rates measured
at four depths (0.5, 1.5, 5, or 10 m, and 20 m beneath thesea ice). The depth of the integrated water column (i.e., 0–20 m) was chosen on the basis of the in-site euphotic zone

Art. 9(1) page 3 of 13

depth. The euphotic zone (>0.415 mol photons m–2 d–1)
was always shallower than 20 m before June 15 and wasapproximately 20 m after June 15 until July 7 (Oziel et al.,2019).
2.4. Diatom composition in the water column

For phytoplankton taxonomy and abundance, 70 mL
water samples were taken from the surface (at 1.5, 5, or
10 m depth) through the 1  1-m sea-ice hole using Niskin bottles on May 25; June 17, 24, 27, and 29; and July 1.
Samples were immediately fixed in 0.3 mL acidified Lugol’s solution for storage until microscopic analyses. At
the laboratory, phytoplankton taxonomy and abundancewere determined by concentrating 70 mL of sample ina sedimentation chamber (Utermöhl, 1931) followed by
identification and counting using a Nikon Eclipse TS100
inverted microscope (as detailed in Lafond et al., 2019).
2.5. Copepod sampling, identification, andestimation of fecal pellet (FP) production andgrazing rates

Zooplankton sampling was conducted through the 1  1m sea-ice hole every 2–7 days between May 24 and July 7,
2016. A 200-mm mesh, 1-m mouth diameter conical net
equipped with a rigid live-capture cod-end was hauledvertically from 100 m (from May 24 to June 21) or 30 m(from June 25 to July 10) to the surface at a towing speedof 0.3 m s–1. The towing depth was changed owing toreasons related to the sampling protocols of other studies,
yet the change minimally affected the results of this study
because the euphotic zone was about 20 m or less during
the study period (Oziel et al., 2019). The filtered volume
was estimated using a digital flowmeter with back-run
stop (KC Denmark, Holmbladsvej, Denmark) mounted
inside the 200-mm mesh net. The filtered volume was anaveraged value from vertical net towing (100 m to thesurface at a towing speed of 0.5 m s–1) on the days immediately before and after sampling (e.g., estimation of thevalue for June 16 was the averaged value of readings onJune 15 and 17) because the towing speed for the experiments was too low to measure the filtered volume. To
remove the effects of variation in the volume filteredbecause of the difference in net towing depth (30 or
100 m), the FP production rate and abundance of copepod
specimens were standardized for those data using a towing
distance of 100 m (i.e., the production rate per square
meter ¼ raw data  100/towing depth). The net was
deployed from the sea-ice hole at around 12:00 (+ 4 h)local time.
After retrieval, live zooplankton were rinsed gently withfiltered (Whatman GF/F glass fiber filter, pore size 0.8 mm)
seawater and sieved into >1 and <1 mm fractions for
incubation. The incubation method followed Sampei etal. (2009). Briefly, each fraction was transferred to a plastic
cylinder immersed in a 1.5-L incubation jar filled withfiltered (Advantec membrane capsule cartridge filter, poresize 0.2 mm) seawater and kept at about 0  C for >12 h.
The bottom of the plastic cylinder was lined with 500-mm
mesh (>1-mm live zooplankton fraction) or 200-mm mesh(<1-mm fraction) to reduce feeding on FPs during the1,634
2,087
130
2,013
508
1,407
828
306
189
1,443
76

785

5,592
6,608
130
11,037
2,532
34,6288,088
816
92
10,171
36

1,347

6,754
6,608
0
10,2893,548
19,392
12,443
1,438
1,051
10,171
508

3,428

1,442
5,283
1,046
696
1,178
117
2,073
3
54
77
12

77

70
13
38
38
318
30
8
156
237
30
0

209

0
0
0
0
0
0
0
0
0
0
0

0

1,415
3,829
417
4,265
6,080
7,389
2,695
625
913
8,351
1,287

1,658

1,162
2,433
0
503
252
2,307
0
0
0
477
0

0

288
183
58
484
199
641
222
46
495
139
48

316

2,333
698
10
2,257
252
922
416
0
66
641
73

3

July 10
July7
July 5
July 2June 30
June 28
June 25
June 21
June 16
June 7

June 11

Sampei et al: copepod grazing pressure on the USPB

May 31incubation. Incubated zooplankton and produced FPs
were picked separately and preserved in buffered formalin(5% v/v) for later microscopic observation. This method
underestimates FP production rate by fragile gelatinous
zooplankton such as appendicularians because they areeasily damaged by plankton nets (Sampei et al., 2009).
FP samples were counted and their dimensions measured (width, length, and shape) under a stereomicroscope(20–40 magnification). FP production rate (mg C m–2 d–1)
was estimated on the basis of geometrical data (produced
FP volume), a gut clearance time of 33 min for Calanus
glacialis stages copepodite V (CV) and copepodite VI (CVI:
adult female) in northern Baffin Bay (Tremblay et al., 2006),
and a conversion factor from FP volume to particulateorganic carbon content of 0.048 + 0.03 mg C mm–3
(González and Smetacek, 1994). The FP production rate wasestimated for four FP width fractions (<50, 50–100, 100–
150, and >150 mm). Zooplankton specimens in a known
aliquot (1.6%–100% of total incubated specimens) containing >200 specimens were counted and identified to species
and developmental stages under a stereomicroscope (10–40 magnification). The main copepod species likely contributing to a given width class of the produced FPs wereidentified on the basis of potential FP producers for a given
width class (Sampei et al., 2009) and their abundance in the
incubated assemblage (ind. m–2; Table 1).
Grazing rate was estimated from the FP production
rate, assuming a digestion efficiency of 70% (Ikeda andMotoda, 1978) as grazing rate ¼ FP production rate 
100/30. Feeding pressure on primary productivity of phytoplankton was further estimated as feeding pressure (%)¼ grazing rate/primary productivity  100. Because no
primary productivity measurements were conducted on
the same days as FP production measurement, primary
productivity on the days of FP production measurement
were interpolated as averaged values of the productivity
on days immediately before and after the date of measurement. All statistical analyses were performed using JSTAT
20.0 J software (Masato Sato, Tokyo, Japan).
3. Results

3,874
346
Others6,597
5,927
Copepod nauplii

9,752
11,855
Oithona similis

9108
Calanus hyperboreus

67
37
M. longa (CIV–VI)

287
0
Metridia longa (CI–III)

9,786
5,148
Pseudocalanus spp. (CIV–VI)

287
224
Pseudocalanus spp. (CI–III)

296
38
C. glacialis (CIV–VI)

0148

3.1. Chl-a concentration and primary productivity
in the water column

Calanus glacialis (CI–III)

May 28May 24
Copepod Species

Table 1. Temporal variabilities (in 2016) of copepod abundances in the incubated copepod assemblages (ind. m–2). DOI: https://doi.org/10.1525/elementa.2019.00092.t1

Art. 9(1) page 4 of 13

The chl-a concentration was low (<1.6 mg chl-a m–3) andstable in the water column (0–40 m depth) between May 24
and June 22. After June 24, chl-a concentration peaked at 20m or shallower depth and stayed relatively high (2.6–7.0 mg
chl-a m–3) until July 8. The column-integrated chl-a biomass(Figure 2) was constantly low (<9.3 mg chl-a m–2) until June
15 and then rapidly doubled (to 20.0 mg chl-a m–2) in 5 days
(between June 15 and 20). The concentration gradually
increased to 219.7 mg chl-a m–2 by the end of the sampling
period (July 8). Temporal variability of the depth-integrated
primary productivity (0–20 m) is shown in Figure 2. The
temporal change was similar to that observed for chla concentration, with stable low primary productivity(<20 mg C m–2 d–1) until June 13 and then a doubling(to 48.4 mg C m–2 d–1) in 7 days (between June 13 and20). Primary production continued to increase rapidlySampei et al: copepod grazing pressure on the USPB

Art. 9(1) page 5 of 13

Figure 2. Temporal variabilities of integrated primary production, chlorophyll-a (chl-a) concentration, and fecal pellet(FP) production rate. Red closed diamonds and green closed triangles show the integrated (0–20 m) primary
production (mg C m–2 d–1) and chl-a concentration (mg chl-a m–2), respectively. Bars show FP production rate (mgC m–2 d–1) for four width ranges (gray: <50 mm and gray stripes sloping up, left to right: 50–100 mm; black: 100–150mm and black stripes sloping up, right to left: >150 mm). DOI: https://doi.org/10.1525/elementa.2019.00092.f2
Table 2. Temporal variability of diatom abundance (cells L–1) in the water column. DOI: https://doi.org/10.1525/
elementa.2019.00092.t2
Sampling Date in 2016 (and Sampling Depth)
May 18May 25June 17

June 24

June 24

June 27

June 29

July 1(1.5 m)(1.5 m)

(5 m)

(5 m)

(10 m)(10 m)(1.5 m)(10 m)

Pseudo-nitzschia spp.
(delicatissima group)

200

400

2,640

296,516

14,1075

552,012258,426

350,428

Pseudo-nitzschia spp.
(seriata group)

0

0

0

15,84015,561

49,22421,09641,020

Fragilariopsis spp.

280

320

7,040

73,80058,653

250,222

173,647.5

69,148Nitzschia spp.

80

1,960

16,720

1,800

513

640

1,370

14,064

Chaetoceros spp.

0

80

120

720

855

11,68030,482.5

54,498

Thalassiosira spp.

0

80

320

560

855

2,080

1,370

1,172

Other diatoms

840

1,812011,88021,24072,846

68,27888,022.5

106,066

Total

1,400

20,96038,720410,476

290,358

934,136

574,414.5

636,396

Diatom Species

until July 6 (661.9 mg C m–2 d–1) and then dropped to166.1 mg C m–2 d–1 by July 8.
3.2. Diatom composition in the water column

The temporal variability of diatom abundance in the watercolumn is shown in Table 2. Nitzschia spp. and Pseudonitzschia spp. were the most dominant diatoms in thecommunity before June 17 and after June 24, respectively.
There was a clear temporal change as the cell numbers ofmost diatoms rapidly increased between June 17 and June
24 (approximately 11-fold increase in total diatoms), andthe abundances remained high until July 1. Potentiallynoxious Pseudo-nitzschia spp. increased from 2,640 cells
L–1 to 312,356 cells L–1 (>100-fold) during the same timeframe. The contribution of Pseudo-nitzschia spp. to thetotal diatom abundance sharply increased from 2%–7%(before June 17) to 49%–76% (after June 24), while thecontribution of Nitzschia spp. decreased from 9%–43%(before June 17) to <1%–2% (after June 24). Thesechanges reflect the quantitative importance of Pseudonitzschia spp. in the diatom community after June 24.
3.3. FP production rate, grazing rate, and feedingpressure

Clear temporal variability was observed for the total FP
production rate (Figure 2). The FP production rate wasconsistently low (<0.9 mg C m–2 d–1) until June 7 andsuddenly increased on June 11 to 3.9 mg C m–2 d–1 when
the integrated chl-a concentration and the integrated primary production were still low. The maximum FP production rate was recorded on June 16 (9.4 mg C m–2 d–1)
before dropping sharply to 0.7 mg C m–2 d–1 on June 21

2
1
<1
2
2
1
1
3
140
90
30

when the integrated chl-a concentration and the integrated primary production began increasing gradually inthe water under the landfast ice. After June 21, the FP
production rate stayed relatively low at <2.8 mg C m–2
d–1, but a second peak was observed on July 2, before
decreasing again despite high and gradually increasing
chl-a concentration and primary production. At least
94% of the FPs produced throughout the study period
was cylindrically shaped (data not shown). The temporalvariability of the FP production rate was inconsistent withthe temporal variability of either the integrated chl-a concentration or primary production. There were no significant relationships between the FP production rate andintegrated chl-a concentration (r ¼ –.213, p > .05, n ¼14) or primary production (r ¼ –.180, p > .05, n ¼ 14).
The contribution of FPs in the width range of 50–150
mm (33%–91%) was generally higher than the contribution of other width range fractions (i.e., <50 mm and >150mm) over the entire study period. The FP width ranges of
50–100 mm and 100–150 mm dominated (89%) the total
FP production on June 16 when the highest FP production
rate was recorded; FPs in the 100–150 mm fraction accounted for 67% of the total produced FPs. The FP width
range of 50–150 mm was also dominant (68%) on June 11
when the second highest FP production rate was recorded;again, the 100–150-mm fraction occupied a substantial
proportion (59%) of the total produced FPs.
Grazing rate (mg C m–2 d–1) and feeding pressure (%)
on primary productivity of phytoplankton (i.e., grazing
rate/primary productivity  100) is presented in Table
3. The grazing rate showed a similar pattern with FP
production rate, given that the grazing rate was estimated based on the FP production rate. The feedingpressure on phytoplankton was one–two orders of magnitude higher before June 11 (30%–146%) than afterJune 21 (<1%–3%).

146

90

38

3.4. Taxonomic composition in the incubatedassemblage

Feeding pressure (%)

3.7
2.6
0.4
9.4
7.1
2.9
1.2
2.4
13.1
1.9
Grazing rate (mg C m –2 d–1)

1.9

1.0

2.8

31.2

166
414
652
474
368
287
122
74.0
22.3
14.6
9.2
1.3
Primary production (mg C m –2 d–1)

2.1

2.6

June 11
May 24

May 28

May 31

June 7

June 16

June 21

June 25

June 28

June 30

July 2

July 5

July 7

July 10Sampei et al: copepod grazing pressure on the USPB

Process

Table 3. Temporal variabilities of interpolated primary production (mg C m–2 d–1), grazing rate (mg C m–2 d–1), and grazing pressure on primary production (%, grazing rate/
primary production  100). DOI: https://doi.org/10.1525/elementa.2019.00092.t2

Art. 9(1) page 6 of 13

Oithona similis, unidentified copepod nauplii, Pseudocalanus spp., C. glacialis, Triconia borealis, and Calanus hyperboreus were the most abundant specimens in the copepod
assemblage (Table 1). Another common large Arctic
copepod species, Metridia longa, also appeared with comparably low abundance. C. glacialis CIV–CVI and M. longa
CIV–CVI had comparably high abundances on June 11 and16 when higher FP production rates were observed. Apartfrom these two copepod groups, no other groups had
higher abundances on June 11 and 16 than on otherdates. A significant positive correlation was observed
between the abundance of C. glacialis CIV–CVI plus M.
longa CIV–CVI and FP production rate (r ¼ .705, p <.01, n ¼ 14). These results highlight the importance of themore mature stages of two large Arctic copepod species
on FP production under the landfast ice.
4. Discussion
4.1. Important contributors to FP production rate

We found a temporal change in the FP production rateduring the conditions of an under sea-ice phytoplankton

Sampei et al: copepod grazing pressure on the USPB

bloom, with the highest FP production rate recorded onJune 16 when chl-a concentration and primary production
were still low. These results raise the question of which
zooplankton species were primarily responsible for thehigh FP production rates on June 11 and 16. Crustaceanssuch as copepods and mysids produce cylindrical FPs(Wexels Riser et al., 2002; Wilson et al., 2008), and>99% of the FPs produced in this study were cylindrical.
Additionally, potential producers of the dominant cylindrical FPs in the width range of 100–150 mm were copepods with prosome lengths of 2.5–3.9 mm (C. glacialis
CIV–CVI, M. longa CIV–CVI, and C. hyperboreus CI–CVI;Sampei et al., 2009), and these copepods were present
at relatively high abundances in the copepod assemblages.
The cylindrical pellets could not have been produced fromthe in vitro predation of large carnivores such as Pareuchaeta glacialis on small copepods because none of thecylindrical FPs from the incubations contained copepod
remnants such as spines (see also Sampei et al., 2009).
Thus, these results, combined with the significant positive
correlation between FP production rate and abundancesof the two large Arctic copepod species, suggest that C.
glacialis CIV–CVI and M. longa CIV–CVI were the main
contributors to FP production. In other words, C. glacialis
CIV–CVI and M. longa CIV–CVI were the main feeders on
phytoplankton in water under the landfast ice.
4.2. Grazing impact on primary production

To quantify grazing impact (i.e., top-down control) on the
primary productivity of under sea-ice phytoplankton, grazing rate, and feeding pressure were estimated in this study(Table 3). The feeding pressure on phytoplankton was>100% on May 24 (146%) and June 16 (140%). These
values may reflect errors in the assumed values for converting FP volume to particulate organic carbon and fordigestion efficiency. These values may also indicate that
ice algae provided an additional food source for copepods
because the presence of ice algae was confirmed by substantial chl-a concentrations in the bottom part (0–3 cm)of the sea ice (5.9 mg m–2 on May 23 and 5.3 mg m–2 onJune 15; Massicotte et al., 2020). A change in ice-algal
biomass, however, is not likely the main factor controllingthe increase in copepod grazing rates between June 11
and 16 (>2 times) and the sudden decrease in the grazing
rate between June 16 and 21 (approximately one-tenth)because the change in chl-a concentration in the sea ice
did not match the change in grazing rate, that is, anapproximate 30% decrease occurred between June 11 and
16 (5.3 mg m–2 and 3.7 mg m–2, respectively) and approximate 10% decrease between June 16 and 21 (3.7 mg m–2
and 3.3 mg m–2, respectively). Sea-ice algal chl-a concentrations were interpolated as described above using chla concentration data from Massicotte et al. (2020) because
no chl-a measurements were conducted on those particular dates. As phytoplankton biomass might remain only 33
min in the gut of copepods (for C. glacialis CV and CVI:
Tremblay et al., 2006), the time lag between feeding andevacuation has no effect on a consideration of this matchor mismatch.

Art. 9(1) page 7 of 13

A clear difference in the feeding pressure wasobserved between May 24 and June 16 when primary
production was still low (1.3–22.3 mg C m–2 d–1) and
June 21 to July 10 (74.0–651.8 mg C m–2 d–1) under the
USPB phase. The feeding pressure before June 16 washigh (30%–146%; average 89%), while the feeding pressure after June 21 was low (<1–3%; average 2%). Thesevariabilities in feeding pressure are consistent witha global comparative analysis indicating that feedingpressure is higher under low primary productivity conditions than under high primary productivity (Calbet,
2001). Grazing pressure has been estimated by previous
studies in Arctic waters (e.g., Nielsen and Hansen, 1995;
Hanse et al., 2003; Tremblay et al., 2006). The feedingpressures from northern Baffin Bay between April andJuly (about 79%; Tremblay et al., 2006), the southeastern
Beaufort Sea in spring–summer (33%–60%; Forest et al.,2011), and Disko Bay during the bloom (80%; Nielsenand Hansen, 1995) were comparable to the higher feeding pressures before June 16 in this study. The feedingpressure from Disko Bay during bloom development(2.9%; Dünweber et al., 2010) and during the sea-ice
breaking period (12%–23%, based on a model calculation; Hansen et al., 2003) were comparable to the lower
feeding pressures after June 21 in this study. Thus, thequantitative impact of copepod grazing (i.e., top-down
control) on primary productivity by the USPB was low,
although copepod grazing could quantitatively impact
the primary productivity of phytoplankton under preUSPB conditions in the water column under landfast ice.
We discuss the possible reasons for the low quantitative
impact of copepod grazing on the USPB primary productivity in Section 4.4.
4.3. Temporal mismatch between copepod grazing
and primary productivity

Match and mismatch scenarios between zooplankton
grazing rate and primary production (see also Sakshaug,2004) have both been reported in Arctic waters (e.g.,Sampei et al., 2004, 2011; Reigstad et al., 2008). The
relationship between grazing rate and primary production clearly showed a mismatch scenario in the present
study. This mismatch (high primary productivity and low
grazing rate after June 20) could flush unconsumed
organic matter from the local surface ecosystem by vertical/horizontal transport (Reigstad et al., 2008) andresult in a slowdown of nutrient supply for regenerated
production in the local surface ecosystem. Zooplankton
feeding releases dissolved inorganic N into the watercolumn, but not dissolved inorganic Si (Dugdale et al.,1995). N limitation occurred and could have restricted
growth of the under sea-ice diatom-dominated phytoplankton. Thus, the low grazing pressure at the beginning to middle of the USPB period (June 20–July 10) may
have served as an additional contributor to the reduction
in total (i.e., new plus regenerated) primary productivity
at the end of the USPB period because of the slowdown
in nutrient regeneration by consumers in the local surface water.

Art. 9(1) page 8 of 13

4.4. Possible causes for the mismatch between
primary production and copepod grazing

The grazing rate and primary production were not significantly correlated (r ¼ –.180, p > .5, n ¼ 14). Two alternative hypotheses exist to explain why the grazing rate did
not increase under higher primary production: low abundance of feeders and low grazing activity owing to a lackof suitable food. The former was not likely the primarycause because the difference in the average abundance ofthe main feeders (i.e., C. glacialis CIV–CVI and M. longa
CIV–CVI) between the periods of June 11–16 and June
21–July 10 (a small difference of 1.8 times: 629 + 146
ind. m–2, n ¼ 2, and 349 + 202 ind. m–2, n ¼ 8, respectively; Table 1) was smaller than the difference in the
average grazing rate of the main feeders, estimated fromthe production rate of FPs in the width range of 100–150
mm (a large difference of 10.2 times: 14.3 + 9.2 mg C m–2
d–1, n ¼ 2, and 1.4 + 1.6 mg C m–2 d–1, n ¼ 8, respectively). The relatively high abundance of the main feeders
from June 21 to July 10 (e.g., 671 ind. m–2 on June 28) was
comparable to those from June 11 to June 16 (525–732
ind. m–2). Moreover, the average abundance of possible
feeders could be much higher in the period of June 21–
July 10 (1,829 + 1,610 ind. m–2, n ¼ 8) than in the periodof June 11–16 (694 + 130 ind. m–2, n ¼ 2) if the otherpossible feeder C. hyperboreus (CI–VI) is included in thecalculation. The increase in the abundance of possible
feeders may be attributable to their seasonal verticalmigration behavior. These copepods could migrate
upward to the surface between June 21 and 25 and staythere until the end of the study period (July 10) because
the seasonal vertical (upward) migration of C. hyperboreus
and C. glacialis occurs when the phytoplankton or ice
algae begin blooming (early May or early April, respectively) in Arctic waters (Darnis and Fortier, 2014). Those
copepods that migrated upward were already actively
grazing and reached peak grazing on June 11–16 in thelocal surface water.
The alternative explanation is that grazing activity was
low because of a lack of suitable food. Phytoplankton size
is an important variable controlling zooplankton grazing,and some species are too small to be grazed efficiently byzooplankton (see Campbell et al., 2009, and references
therein). However, the contributions of small phytoplankton species (flagellates and dinoflagellates) to thetotal phytoplankton abundance were as low as 14% (May23), 5% (June 17), 9% (June 24), 4% (June 27), 20% (June29), and 10% (July 1) at a depth of 5 m below the sea ice(PL Grondin, personal communication, 2019). These low
contributions suggest that low grazing pressure during
the USPB did not result from the dominance of small
phytoplankton in the water column. The phytoplankton
species composition in the water column changed drastically after June 20 (PL Grondin, personal communication, 2019). Our results clearly show that the abundanceof Pseudo-nitzschia spp. increased from 0.4–2.6  103
cells L–1 to 1.6–6.0  105 cells L–1 in the surface (1.5–
10 m) water under the landfast ice. The average contribution of Pseudo-nitzschia spp. to the entire populationof diatom cells also increased by more than one order ofSampei et al: copepod grazing pressure on the USPB

magnitude, from 4% (n ¼ 2) to 61% (n ¼ 5). Furthermore, the average contribution of Pseudo-nitzschia spp.
to the total phytoplankton cell abundance could be estimated as 1% (May 25), 3% (June 17), 21%–29% (June24), 34% (June 27), 24% (June 29), and 33% (July 1) on
the basis of the contribution of diatoms to the total
phytoplankton abundance (PL Grondin, personal communication, 2019). The contribution of Pseudonitzschia spp. to total phytoplankton cell biomass could
be higher than that of their numerical abundance
because the contribution of diatoms to total phytoplankton biomass (mean + standard deviation: 68 + 10%, n¼ 6) was also significantly higher than that of their abundance (45 + 10%, n ¼ 6) (PL Grondin, personal communication, 2019). Pseudo-nitzschia spp. can produce theneurotoxin domoic acid, though only half of the species
have been reported as domoic acid producers (Bates etal., 2018) and only Pseudo-nitzschia arctica, which has
never been reported as a domoic acid producer, is present in the Baffin Bay (Ribeiro et al., 2020). Yet, all strainsof Pseudo-nitzschia spp. may eventually prove to be domoic acid producers (Bates et al., 2018). Pseudo-nitzschia
obtusa, which was initially considered a nontoxic species,
was later found to be a domoic acid producer (Harðardóttir et al., 2015). Domoic acid production is a chemical
defense mechanism against predation (Harðardóttir etal., 2018), and ingestion of the neurotoxin can negatively
affect the physiological activities of calanoid copepods
like C. hyperboreus and C. glacialis (Tammilehto et al.,2012). For example, C. hyperboreus stopped grazing 6 hafter commencing grazing on Pseudo-nitzschia (Tammilehto et al., 2012), though Harðardóttir et al. (2015)
found no negative impact of domoic acid on copepod
grazing over a longer term (8–10 days) and previous
studies found no negative impact on copepod grazing(Lincoln et al., 2001; Maneiro et al., 2005; Leandro etal., 2010). Moreover, ingestion of domoic acid reduced
the escape responses of C. hyperboreus and C. glacialis(Harðardóttir et al., 2018). Thus, the large increase inabundance of Pseudo-nitzschia spp. might explain the
low grazing rate under the USPB conditions. This explanation is consistent with the individual grazing rates ofpotential feeders (C. glacialis CIV–CVI, M. longa CIV–CVI,and C. hyperboreus CI–VI) from June 21 to July 10 (0.7 mg
C ind.–1 d–1) being lower than the rates during the periodof June 11–16 (20.6 mg C ind.–1 d–1), where rates were
calculated using the estimated grazing rates for these
copepods and their abundances.
5. Conclusions
With intense temporal coverage (once every 2–3 days) of
field sampling and comprehensive data sets (e.g., phytoplankton taxonomy, light profiles, and nutrient concentrations) from the Green Edge project from the end of May tothe beginning of July (from pre-USPB and progressing into
the USPB period), this study successfully illustrated finescale temporal variability of grazing impact on phytoplankton and investigated possible processes controllinggrazing under landfast sea ice. In summary:Sampei et al: copepod grazing pressure on the USPB

1. Low grazing pressure on phytoplankton during the USPB phase (i.e., mismatch scenario)
indicated that copepod grazing did not control daily growth of phytoplankton under the
USPB condition, although copepod grazing
may have affected the productivity of phytoplankton under pre-USPB conditions.
2. This mismatch scenario might occur becauseof food quality (i.e., appearance of potentiallytoxigenic diatoms) rather than abundance ofgrazers in the surface water under landfast
sea ice.
3. The main grazers were large dominant Arctic
copepods—C. glacialis, M. longa, and C. hyperboreus—rather than small copepods suchas Pseudocalanus spp., which are the maingrazers in water under landfast sea ice inshallow Canadian Archipelago waters (100–150 m depth; Fortier et al., 2002).
4. Ongoing climate change could bring thinnersea ice, longer open water periods, and lesssnowfall in the Arctic (Bintanja et al., 2018;
Stroeve and Notz, 2018). These environmental changes increase light availability, which
affects microalgal growth, and further benefit
phytoplankton, rather than ice algae, beneaththe sea-ice cover in Baffin Bay (Oziel et al.,2019). These changes suggest that preyaccessibility for the main grazers increases inthe surface water under sea ice because thesinking speed of phytoplankton (diatoms,<1–35 m d–1; Miklasz and Denny, 2010) is 1–
2 orders of magnitude slower than that ofaggregated ice algae (100–500 m d–1; Riebesell et al., 1991), and aggregated microalgae
are not favorable prey particles for grazers(Lürling and Van Donk, 1996). However, thepresent study indicates that grazers simply
could not catch up with the increase in primary production by phytoplankton under thesea ice (i.e., during the USPB). We speculatethat grazing pressure on phytoplankton will
not increase as expected with an increase in
USPB in Baffin Bay, but further studies are
required to predict grazing pressure on phytoplankton under the sea ice.

Data accessibility statement
All data are accessible at the Green Edge database (http://
www.obs-vlfr.fr/proof/php/GREENEDGE/greenedge.php)
and will be made public prior to publication.

Art. 9(1) page 9 of 13

Acknowledgments
This project would not have been possible without the
support of the hamlet of Qikiqtarjuaq and the membersof the community as well as the Inuksuit School and its
principal Jacqueline Arsenault. The community contributed to the scientific campaign by facilitating logisticalsupport and sharing local knowledge. The project was conducted under the scientific coordination of the Canada
Excellence Research Chair in Remote Sensing of Canada’s
New Arctic Frontier and the French Centre National de laRecherche Scientifique and Laval University Takuvik Joint
International laboratory (UMI3376). The field campaign
was successful thanks to the contribution of J. Ferland,
G. Bécu, C. Marec, J. Lagunas, F. Bruyant, J. Larivière, E.
Rehm, S. Lambert-Girard, C. Aubry, C. Lalande, A. LeBaron,
C. Marty, J. Sansoulet, D. Christiansen-Stowe, A. Wells, M.
Benoı̂t-Gagné, E. Devred, and M.-H. Forget from the Takuvik Laboratory, C.J. Mundy and V. Galindo from Universityof Manitoba, as well as F. Pinczon du Sel and E. Brossierfrom Vagabond. We also thank Michel Gosselin, QuébecOcéan, the CCGS Amundsen, and the Polar Continental
Shelf Program for their in-kind contribution in polar logistic and scientific equipment. We also thank P.L. Grondinfor kindly sharing unpublished phytoplankton taxonomic
and nutrient data. We are grateful to three anonymous
reviewers and an editor for valuable comments and suggestions on an earlier version of the manuscript. We thankCatherine Dandie, PhD, and Natalie Kim, PhD, from Edanz
Group (https://en-author-services.edanzgroup.com/ac)
for editing a draft of this manuscript. This is a contribution
to the Arctic Challenge for Sustainability (ArCS), the Green
Edge, and the Canada Research Chair on the response ofmarine Arctic ecosystems to climate warming.
Funding
The Green Edge project is funded by the following French
and Canadian programs and agencies: ANR (Contract#111112), CNES (project #131425), IPEV (project#1164), CSA, Fondation Total, ArcticNet, LEFE, and theFrench Arctic Initiative (Green Edge project). M. Sampei
K. Matsuno, Y. Abe, and T. Hirawake are funded by Ministryof Education, Culture, Sports, Science and Technology ofJapan through the ArCS project.
Competing interests
The authors have no competing interests to declare.
Author contributions
Contributed to design of the article: MS, LF, MB, TH.
Contributed to sampling and analysis: MS, PR, BQ, YA,
AL.
Drafted the article: MS, KM.
Contributed to the discussion and revision of early versions of the article: All authors.
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Art. 9(1) page 13 of 13

How to cite this article: Sampei, M, Fortier, L, Raimbault, P, Matsuno, K, Abe,Y, Quéguiner, B, Lafond, A, Babin, M, Hirawake, T.
2021. An estimation of the quantitative impacts of copepod grazing on an under sea-ice spring phytoplankton bloom inwestern Baffin Bay, Canadian Arctic. Elementa: Science of Anthropocene 9(1). DOI: https://doi.org/10.1525/
elementa.2019.00092
Domain Editor-in-Chief: Jody W. Deming, University of Washington, Seattle, WA, USA
Associate Editor: Kevin Arrigo, Department of Earth System Science, Stanford University, Stanford, CA, USA
Knowledge Domain: Ocean Science
Part of an Elementa Special Feature: Green Edge
Published: June 11, 2021

Accepted: April 29, 2021

Submitted: December 27, 2019

Copyright: © 2021 The Author(s). This is an open-access article distributed under the terms of the Creative Commons
Attribution 4.0 International License (CC-BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium,provided the original author and source are credited. See http://creativecommons.org/licenses/by/4.0/.

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