ICES Journal of Marine Science (2020), 77(2), 711–720. doi:10.1093/icesjms/fsz213

Contrasting assemblages of seabirds in the subglacial meltwaterplume and oceanic water of Bowdoin Fjord,
northwestern Greenland
Bungo Nishizawa 1*, Naoya Kanna2, Yoshiyuki Abe3, Yoshihiko Ohashi4,5, Daiki Sakakibara2,
Izumi Asaji4,5, Shin Sugiyama2,4, Atsushi Yamaguchi2,6, and Yutaka Watanuki2,61

National Institute of Polar Research, Midori-cho 10-3, Tachikawa, Tokyo 190-8518, Japan
Arctic Research Center, Hokkaido University, Kita-21 Nishi-11 Kita-ku, Sapporo, Hokkaido 001-0021, Japan
3
Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwanoha, Kashiwa, Chiba 277-8564, Japan
4
Institute of Low Temperature Science, Hokkaido University, Kita-19, Nishi-8, Kita-ku, Sapporo, Hokkaido, 060-0819, Japan
5
Graduate School of Environmental Science, Hokkaido University, Sapporo, Hokkaido 060-0810, Japan
6
Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1, Minato, Hakodate, Hokkaido 041-8611, Japan
2*Corresponding author: tel: (þ81) 138-40-8863; e-mail: nishizawa@salmon.ﬁsh.hokudai.ac.jp.
Nishizawa, B., Kanna, N., Abe, Y., Ohashi, Y., Sakakibara, D., Asaji, I., Sugiyama, S., Yamaguchi, A., and Watanuki, Y. Contrasting assemblages of seabirds in the subglacial meltwater plume and oceanic water of Bowdoin Fjord, northwestern Greenland. – ICES Journal of
Marine Science, 77: 711–720.
Received 3 March 2019; revised 11 October 2019; accepted 15 October 2019; advance access publication 14 December 2019.
In Greenland, tidewater glaciers discharge turbid subglacial freshwater into fjords, forming plumes near the calving fronts, and these areas
serve as an important foraging habitat for seabirds. To investigate the effect of subglacial discharge on the foraging assemblages of surface
feeders and divers in a glacial fjord, we conducted boat-based seabird surveys, near-surface zooplankton samplings, and hydrographic measurements at Bowdoin Fjord, northwestern Greenland in July. Foraging surface feeders (black-legged kittiwake Rissa tridactyla, glaucous gull
Larus hyperboreus, and northern fulmar Fulmarus glacialis) aggregated within a plume-affected area in front of Bowdoin Glacier. This area wascharacterized by highly turbid subglacial meltwater and abundant large-sized zooplankton including Calanus hyperboreus, chaetognaths, andctenophores near the surface. Surface feeders fed on these aggregated prey presumably transported to the surface by strong upwelling of subglacial meltwater. In contrast, divers (little auk Alle alle, thick-billed murre Uria lomvia, and black guillemot Cepphus grylle) foraged outside
the fjord, where turbidity was low and jellyﬁsh and Calanus copepods dominated under the inﬂuence of Atlantic water. Our study indicatesspatial segregation between surface feeders and divers in a glacial fjord; surface feeders are not hindered by turbidity if taking prey at the surface, whereas divers need clear water.
Keywords: divers, fjord, surface feeders, tidewater glacier, turbidity, upwelling

Introduction
The mass loss of glaciers is accelerating worldwide because of
global warming (Bliss et al., 2014). Glacial meltwater provides
sediment-laden freshwater and has the potential to alter the physical and chemical properties of the adjacent sea and marine ecosystems. For example, the freshwater runoff from Alaskan glaciers
affects large-scale circulation and primary productivity in the

coastal waters of the Gulf of Alaska (Weingartner et al., 2005), as
well as in the fjords (Etherington et al., 2007). Within fjords, theestuarine circulation, driven by the summer glacial meltwater discharge, transports various zooplankton species with near-bottom
currents towards the glacier front where they may be advected tothe surface (We˛sławski et al., 2000). Therefore, marine predators
including fish, seabirds, and marine mammals tend to aggregate to

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Original Article

712

from the glacier front. To test these hypotheses, we examined (i)the effect of turbidity (a proxy for glacial meltwater) on the density of foraging surface feeders and (ii) the effect of turbidity on
the density of foraging divers.

Material and methods
Study area and sampling overview
Bowdoin Glacier (77 410 N, 68 350 W) is a marine-terminating
outlet glacier (i.e. tidewater glacier) located in northwestern
Greenland (Figure 1). The glacier discharges into Bowdoin Fjord
through a 3-km wide calving front. The height of the calving
front above the sea surface is between 20–25 m (Sugiyama et al.,2015). At 20 km south of the calving front, Bowdoin Fjord connects to Inglefield Bredning, the largest fjord in this region. In
turn, Inglefield Bredning Fjord connects to the western part of
Baffin Bay, where warm, saline, and northward-flowing Atlantic
water, called West Greenland Current, exists. In front of the glacier centre within 2 km of the terminus, the sea depth ranges between 190 and 210 m (Sugiyama et al., 2015). The sea depth
deepens towards the mouth of the fjord, which has no sill, where
the average sea depth is 500 m (Sugiyama et al., 2015). Recently,
Bowdoin Glacier retreated rapidly with a significant accelerationin ice flow speed (Sugiyama et al., 2015).
The at-sea field surveys were conducted in calm weather on 27
and 29 July 2016 at Bowdoin Fjord in the northwestern
Greenland. Sea ice covering the entire fjord began disintegratingin early July and completely disappeared from the fjord before
our surveys (approximately on 23 July 2016). Small icebergs weresparsely distributed in the fjord during our survey periods, butthey did not disturb our ship navigation and observations. Twosmall boats of 5 m length were operated in the fjord; one boat wasfor conductivity-temperature-depth (CTD) observations and surface seawater samplings, and the other one for seabird observations and near-surface zooplankton samplings.

Seabird observations
The at-sea seabird observations were conducted on 27 and 29 July
2016 in Bowdoin Fjord (Figure 1), concurrently with zooplankton
samplings. We used the standard strip transect methodology(Tasker et al., 1984) while the vessel was underway. During ourobservations, a single observer continuously recorded the number
and behaviours (flying, sitting on water, sitting on iceberg, and foraging) of all seabirds using the 8 binoculars (eye height above sea
surface of 2 m) within a 200-m survey range (from the bow to 90
to port or to starboard) of the side of the boat that offered the best
observation conditions (i.e. the lowest sun glare) during daylight
hours. The position (latitude and longitude) of the boat during theobservations was obtained at 30-s intervals using a handy GPS(eTrex venture HC manufactured by GARMIN). We defined surface feeders sitting on water or foraging as “foraging surface
feeders” because they feed on prey at the surface by surface-seizing
or surface-plunging (<1 m). We also defined divers sitting on water as “foraging divers” because they were assumed to be about toforage or to be resting from a previous foraging bout (Hunt et al.,
1998; Kokubun et al., 2008). Seabirds flying or sitting on icebergs
were considered as “non-foraging” in our study. The density ofseabirds was defined as the number of individuals per 200  200 mcell, which is the highest resolution in our study. We chose this cellsize because our study area of Bowdoin Fjord is relatively small(i.e. 3-km wide  20-km long). The total time of seabird surveys

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feed at the front of tidewater glacier (Hop et al., 2002; Lydersen
et al., 2014; Arimitsu et al., 2016; Dalpadado et al., 2016).
Tidewater glacier fronts are known as an important foraging
habitat for seabirds (Lydersen et al., 2014). In western Baffin Bay
and eastern Lancaster Sound, Canada, for instance, the densities
of surface-feeding seabirds, black-legged kittiwakes (Rissa tridactyla), ivory gulls (Pagophila eburnea), and northern fulmars(Fulmarus glacialis), were significantly higher in front of glaciers
than along coastlines during summer and fall (McLaren andRenaud, 1982; Renaud and McLaren, 1982). Previous studies inWest Spitsbergen showed that, in summers, large aggregations ofblack-legged kittiwakes and northern fulmars occurred in meltwater plumes near the front of tidewater glaciers, where they fed
on macroplankton, such as krill (Thysanoessa spp.) and amphipods (Hartley and Fisher, 1936; Stott, 1936). A recent study
revealed that zooplankton is transported to the surface as a partof the large volume of ambient water entrained by rising plumesof subglacial discharge, thereby making them more easily accessible for surface feeders (black-legged kittiwakes; Urbanski et al.,2017). The locations and magnitudes of these subglacial discharges fluctuate in time, thereby affecting the locations of theaggregations of surface-feeding kittiwakes (Urbanski et al., 2017).
In contrast to surface feeders, pursuit-diving seabirds, such as
little auks (Alle alle) and thick-billed murres (Uria lomvia), weregenerally absent from the areas in front of tidewater glaciers(Hartley and Fisher, 1936; Stott, 1936). Despite these previously
reported observations of foraging seabirds, the responsible mechanism is still unknown. One possible interpretation is that the
turbid meltwater from tidewater glaciers prevents prey detection
by divers at depth (Ainley, 1977; Lydersen et al., 2014). In Prince
William Sound, Alaska, two pursuit-diving alcids (Kittlitz’s murrelets Brachyramphus brevirostris and marbled murrelets B. marmoratus) exhibited differences in habitat use; Kittlitz’s murrelets
preferred turbid glacial water, while marbled murrelets preferred
clearer water without glacial influence (Day and Nigro, 2000; Dayet al., 2003). Kittlitz’s murrelets have proportionately largerdiameter eyes than those of marbled murrelets, which might allow them to capture prey in silty water (Day et al., 1999). Since
2005, after the disappearance of summer sea ice and the increasein coastal glacial meltwater in Franz-Josef Land (80 N), Russian
Arctic, little auks have switched foraging sites from ice-edge waters located at a long distance from their breeding site to glacial
meltwater fronts within <5 km of their breeding site (Grémillet
et al., 2015). Thus, the ways in which glacial meltwater influences
the foraging habitats of divers vary among localities and species.
To understand the factors affecting seabird foraging aggregations in glacial fjords, boat-based seabird observations, hydrographic measurements, and near-surface zooplankton (i.e.
seabird’s main prey) samplings were performed in Bowdoin
Fjord, a glacial fjord in northwestern Greenland, in the summerof 2016. During our summer field research activities, carried out
in this region since 2013, large seabird aggregations have been frequently observed at the front of tidewater glacier. We compared
foraging distributions between surface feeders and divers in relation to oceanographic environments, with special attention toturbidity and prey distributions. We hypothesized that surface
feeders forage at the front of the tidewater glacier where theirprey, large zooplankton, are transported to the near surface by
upwelling of a turbid subglacial discharge plume. On the other
hand, divers were expected to avoid turbid meltwater plume at
the front of the tidewater glacier and forage in clear water away

B. Nishizawa et al.

Contrasting assemblages of seabirds

713

was 504 min (278 min on 27 July and 226 min on 29 July). The total number of seabird sampling cells (i.e. 200  200 m) was 521(284 on July 27 and 237 on July 29).

Zooplankton sampling
Near-surface zooplankton was collected during daytime on 27
and 29 July 2016, concurrently with seabird observations, at 15

sampling stations (six stations on 27 July and nine stations on 29
July, Figure 1, data from Naito et al., 2019) from the outside of
Bowdoin Fjord (23 km from the calving front of Bowdoin Glacierand 4 km from the exit of the fjord) to the front of Bowdoin
Glacier (200 m from the calving front of Bowdoin Glacier). The
sampling was performed by horizontal tows with a North PacificStandard Net (NORPAC net; mouth diameter 45 cm, mesh size
335 lm, Motoda, 1957) at a depth of 1.0–2.5 m for 3 min at a

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Figure 1. Study area with seabird observation lines (circles), CTD stations (diamonds) with station name (C number), and zooplankton
sampling stations (triangles) with station name (Z number). Study area of Bowdoin Fjord in northwestern Greenland (a), details inside fjord(b), the plume-affected at the front of Bowdoin Glacier (c), and outside fjord (d). Arrows denote proglacial streams from land-terminating
glaciers. Maps are the natural-color images taken from satellite on July 30 2016.

714

Oceanographic measurements and seawater sampling
Surface seawater temperature (resolution 0.001 C) and turbidity[resolution 0.03 FTU (formazin turbidity unit)] were measured
at the depth of 0.3 m by a CTD profiler (JFE Advantech Co., Ltd.,RINKO-Profiler ASTD102) on-board the boat. The measurements were performed on 27 July at 44 stations in Bowdoin Fjord
from the mouth of the fjord to the calving front of Bowdoin
Glacier (0.25–23 km from the glaciers, Figure 1, data from Kanna
et al., 2018). Surface water sampling was conducted at the CTD
stations to measure the salinity. The salinity of the surface water
was determined using a salinometer (AUTOSAL 8400B, Guildline
Instruments, USA; instrumental accuracy: <0.002). Hereafter, theCTD stations will be described as “C number”.

Analyses
Our 2 d (on 27 and 29 July) of observations of seabird and zooplankton samplings were pooled into a single dataset, because thespatial patterns of seabirds were similar for the 2 d (i.e. during
both days the highest densities of divers and surface feeders occurred in outside fjord and plume-affected sections, respectively)
and the number of the zooplankton sampling stations was small(six stations on 27 July and nine stations on 29 July). Note here
again that CTD observations were conducted only on 27 July. In
our analysis, we excluded skuas and common eiders (Somateria
mollissima) from surface feeders or divers because skuas are kleptoparasitic and feed by stealing fish and other prey from otherseabirds, such as gulls and terns, and common eiders feed mainly
on benthos, such as bivalves and polychaetes (Merkel et al., 2007;
Supplementary Table S1).
To explore the relationships among seabird density, turbidity,
and abundance of zooplankton, we compared the data from three

sections in the study area. We defined the section within 2 km
from Bowdoin Glacier (C1–C18) as a “plume-affected” since surface water showed high turbidity (i.e. >5 FTU) in this section(Figures 2 and Supplementary Figure S3). The section between
the plume-affected section and the mouth of Bowdoin Fjord(19 km from Bowdoin Glacier) was defined as “inside fjord” andthe section on the outside of Bowdoin Fjord as “outside fjord”.
We then compared the seabird densities, abundances of large andsmall zooplankton, and surface oceanographic environments (water temperature, salinity, and turbidity) among these three sections using the Steel-Dwass pairwise non-parametric test. Values
are expressed as mean 6 SD.
Based on the finer spatial resolution data obtained at eachsampling station, we examined our above-mentioned hypotheses
using non-parametric generalized additive models (GAMs). To
examine the effect of turbidity on the density of foraging surface
feeders and foraging divers, we used turbidities at 44 CTD stations, and the total abundance of foraging surface feeders and divers that occurred within 1 km area from each CTD station. In
these GAMs, response variables, such as seabird abundance, wereassumed to be negative binomial distributions with log link functions because the data were overdispersed. Moreover, owing to an
unequal survey length of seabird observations within the 1 km
area from each CTD station, survey effort (i.e. the total survey
length in each 1 km area) was treated as an offset term in the
GAMs. GAMs were implemented using the mgcv package in thefree statistical analysis software R (v.3.1.2, R Development Core
Team, 2014) using generalized cross-validation to estimate
smoothness parameters (Zuur et al., 2009).
The position of the calving front of Bowdoin Glacier was measured on a natural-colour satellite image from Landsat 8 (bands
4, 3, and 2 were synthesized) on July 30, 2016 (downloaded fromhttp://earthexplorer.usgs.gov/). The spatial resolution of the image was 30 m.

Results
We observed nine seabird species (Supplementary Table S1).
Surface feeders included black-legged kittiwake, glaucous gull,and northern fulmar, with black-legged kittiwake being the mostabundant (91%; Supplementary Table S1). Divers included little
auk, thick-billed murre, and black guillemot, with little auk being
the most abundant (80%; Supplementary Table S1).
We collected 20 zooplankton species (Supplementary Table
S2). Large zooplankton (>5 mg ind.1) included jellyfish (cnidarians and ctenophores), chaetognaths, appendicularians, thecosomes, and Calanus hyperboreus (Supplementary Table S2).
Barnacle larvae, classified as small zooplankton (<5 mg ind.1),
were collected at all sampling stations and accounted for 6–100%
in abundance and <1–87% in biomass.

Comparison between sections
Plume-affected section
The density of foraging surface feeders in the plume-affected section at the front of Bowdoin Glacier was the highest among thethree sections (Table 1, Figure 3a). A huge mixed-aggregation of
black-legged kittiwakes (930 birds per 200 m2) and glaucous gulls(100 birds per 200 m2) was observed within 300 m from the glacier front. These birds exhibited repeated foraging behaviours,
such as surface-seizing or surface-plunging. We also observed atleast 10 black-legged kittiwakes in the aggregated birds capturing

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ship speed of 5 km h1. The volume of water filtered through the
net was estimated using a flow-meter mounted in the mouth of
the net. On the mouth of the net, a 6-kg weight and floater (distance between the net mouth and the floater was 1.35 m) were attached, allowing us to tow the net horizontally in the near-surface
layer. The distance from the stern to the net was 20 m when hauling, thereby avoiding the effect of turbulence by the boat propeller during our zooplankton sampling. The net depth wasrecorded every second with a depth logger (JFE Advantech Co.,
Ltd., DEFI2-D50, 0.05 m resolution) attached on the mouth of
the net. The zooplankton samples were immediately fixed with
4% buffered formalin seawater on the boat. In the laboratory,
species identification and enumeration were performed under astereomicroscope. Subsequently, we weighed the wet mass (WM)of each taxonomic group with a precision of 0.1 lg using an electronic balance (Mettler AE-100). The zooplankton biomass (X:mg WM m3) was calculated based on the WM and volume ofwater filtered through the net.
In the fjord on the west coast of Spitsbergen, black-legged kittiwakes feed on large zooplanktons (>5 mg individual WM) abundantly distributed in the vicinity of glacier cliffs (Urbanski et al.,2017). We thus defined “large zooplankton” (mean individual
WM >5 mg) and “small zooplankton” (mean individual WM<5 mg) based on the individual mean WM calculated from thebiomass and abundance of each taxonomic group. Thereafter, we
examined the abundance of large and small zooplankton at eachsampling station. Hereafter, the zooplankton sampling stations
will be described as “Z number”.

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Contrasting assemblages of seabirds

fish (probably polar cod Boreogadus saida, 15 cm in the total
length, Supplementary Figure S1). The non-foraging (flying or
sitting on iceberg) surface feeders in this section also showed thehighest density (Table 1, Supplementary Figure S2a). On theother hand, no divers, whether foraging or non-foraging, wereobserved in the plume-affected section (Table 1, Figure 3b,
Supplementary Figure S2b).
The zooplankton abundance collected in near-surface water
was highly variable between the stations (Figure 2a). The averageabundance and biomass of total zooplankton in the plumeaffected section were similar with those in the inside fjord section(Table 1). The average abundance of large zooplankton, however,seemed to be the highest among the three sections, although thetrend was not significant (Table 1, Figure 2a). The large zooplankton (stations Z1–Z5) included ctenophores, chaetognaths(Parasagitta elegans and Eukrohnia hamata), fish larvae, andcopepods (Calanus hyperboreus; Supplementary Table S2).
The average surface water temperature in the plume-affected
section was the highest, while the surface salinity was the lowest(Table 1, Figure 2b and Supplementary Figure S3). The surface

turbidity was the highest, especially at the stations of C3–C8(Table 1, Figure 2c and Supplementary Figure S3).

Inside fjord section
The densities of both foraging and non-foraging surface feeders
and divers in the inside fjord section were quite low (Table 1,
Figure 3 and Supplementary Figure S2).
The average abundance and biomass of total zooplankton in
the inside fjord were similar with those in the plume-affected section and the large zooplankton seemed to be a low abundance, although the trend was not significant (Table 1 and Figure 2a).
Among zooplankton sampling stations in the inside fjord, station
Z10 showed the highest density of small zooplankton (Figure 2a),with barnacle larvae as the dominant zooplankton species(Supplementary Table S2).
The average surface water temperature in the inside fjord was
lower than that in the plume-affected section and decreased gradually towards the outside fjord section, while the surface salinity
showed an opposite trend (Table 1, Figure 2b and Supplementary

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Figure 2. Zooplankton abundance and oceanographic environments in Bowdoin Fjord (plume-affected and inside and outside fjord sections)in northwestern Greenland. Large (>5 mg mean individual WM) and small (<5 mg mean individual WM) zooplankton abundances (a), sea
surface temperature (SST) and salinity (b), turbidity (c).

Non-foraging

Foraging

Non-foraging

Foraging

Plume-affected
14.1 6 109.2(0.0–1030.0), n ¼ 88
4.2 6 17.3
(0.0–150.0), n ¼ 88
0
n¼ 88
0
n¼ 88
1332.2 6 1512.6(39.9–4199.4), n ¼ 5
50.9 6 30.0
(13.3–90.8), n ¼ 5
2.9 6 3.1
(0.2–7.8), n ¼ 51328.5 6 1509.3(34.6–4187.9), n ¼ 5
5.1 6 0.2
(4.7–5.4), n ¼ 18
12.5 6 2.2(7.9–15.2), n ¼ 18
7.1 6 3.0
(5.0–17.1), n ¼ 18

Inside fjord
0.1 6 1.1
(0.0–20.0), n ¼ 317
0.3 6 0.7
(0.0–4.0), n ¼ 317
0.0 6 0.3
(0.0–3.0), n ¼ 317
0.1 6 0.3
(0.0–4.0), n¼3171456.9 6 2390.9(7.1–7579.4), n ¼ 8
65.0 6 78.1
(4.0–259.1), n ¼ 8
0.9 6 0.8
(0.0–2.3), n ¼ 81455.9 6 2391.0(6.2–7579.0), n ¼ 8
4.4 6 0.5
(3.2–5.2), n ¼ 24
21.1 6 2.8(15.4–27.0), n ¼ 24
4.3 6 2.8
(1.4–15.0), n ¼ 24

Outside fjord
0.0 6 0.2
(0.0–0.2), n ¼ 116
0.5 6 0.8
(0.0–4.0), n ¼ 116
3.0 6 8.0
(0.0–50.0), n ¼ 116
0.6 6 1.6
(0.0–13.0), n ¼ 116
41.5 6 23.8
(17.7–65.2), n ¼ 2
22.8 6 7.9(15.0–30.7), n ¼ 2
0.7 6 0.1
(0.6–0.8), n ¼ 2
40.7 6 23.9
(16.9–64.6), n ¼ 2
4.5 6 1.0
(3.4–5.5), n ¼ 2
28.0 6 2.5(25.5–30.5), n ¼ 2
1.2 6 0.6
(0.6–1.7), n ¼ 2

Inside fjord
vs. Outside fjord
0.7, p ¼ 0.78
1.6, p ¼ 0.24
8.7, p < 0.05
5.9, p < 0.05
1.0, p ¼ 0.55
0.5, p ¼ 0.86
0.5, p ¼ 0.86
1.0, p ¼ 0.55
0.1, p ¼ 0.10
2.0, p ¼ 0.11
2.2, p ¼ 0.08

Plume-affected
vs. Outside fjord
3.5, p < 0.05
2.8, p < 0.05
6.0, p < 0.05
4.6, p < 0.05
1.5, p ¼ 0.27
0.7, p ¼ 0.72
0.4, p ¼ 0.92
1.5, p ¼ 0.27
0.0, p ¼ 1.00
2.3, p ¼ 0.06
2.3, p ¼ 0.06

Plume-affected
vs. Inside fjord
5.7, p < 0.05
4.8, p < 0.05
1.9, p ¼ 0.15
1.9, p ¼ 0.15
0.4, p ¼ 0.90
0.7, p ¼ 0.74
0.6, p ¼ 0.83
0.4, p ¼ 0.90
5.5, p < 0.05
5.5, p < 0.05
4.2, p < 0.05

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Values are described in mean 6 SD, range, and sample size.

Turbidity (FTU)

Salinity

Total zooplankton abundance(ind. m3)
Total zooplankton biomass(mg WM m3)
Large zooplankton abundance(ind. m3)
Small zooplankton abundance(ind. m3)
SST (oC)

Density of divers(ind. 200 m2)

Variables
Density of surface feeders(ind. 200 m2)

Steel-Dwass test (t-statistics, p-value)

Table 1. Density of surface feeders, density of divers, zooplankton abundance (ind. m3), and zooplankton biomass (mg WM m3), sea surface temperature (SST,  C), salinity, turbidity[formazin turbidity unit (FTU)] between three sections (plume-affected, inside fjord, and outside fjord), and the results of the Steel-Dwass test (t-statistics and p-value).

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Contrasting assemblages of seabirds

Figure S3). The average surface turbidity in the inside fjord
showed intermediate values among the sections, with high values
recorded at the stations of C36–C38 (12–14 km away from theglacier; Table 1, Figure 2c and Supplementary Figure S3).

Discussion
Our study indicated that surface feeders and divers used different
foraging habitats with almost no spatial overlap in Bowdoin
Fjord, and this segregation was correlated with the varying turbidity level of the subglacial meltwater.

Outside fjord section
The density of foraging surface feeders in the outside fjord section
was low as observed in the inside fjord (Table 1 and Figure 3a),while the density of foraging divers was the highest (Table 1 andFigure 3b). Similarly, the density of non-foraging surface feeders
was low, while the density of non-foraging divers was the highest(Table 1 and Supplementary Figure S2).
The average abundance and biomass of total zooplankton in
the outside fjord seemed to be the lowest (Table 1 and Figure 2a).
The average surface water temperature in the outside fjord
showed a value similar to that in the inside fjord with high variability between the stations, while the surface salinity was thehighest among the sections (Table 1, Figure 2b andSupplementary Figure S3). The surface turbidity measurementsin this section were the lowest (Table 1, Figure 2c andSupplementary Figure S3).

Effect of turbidity on the density of surface feeders and divers
The turbidity had a positive effect on the density of foraging surface feeders; in the vicinity of the stations where the turbidity was
high, the density of the foraging surface feeders was also high(Figure 4a). On the other hand, the turbidity had a negative effecton the density of foraging divers (Figure 4b).

Foraging habitat of surface feeders
In the turbid subglacial meltwater plume near the front of
Bowdoin Glacier, surface feeders, including the black-legged kittiwake, northern fulmar, and glaucous gull, aggregated for feeding.
In this area, the abundance of large zooplankton (>5 mg ind.1)
in near-surface water tended to be higher than in the inside andoutside fjord sections. Although the diets of the seabirds were unknown in the present study, they probably fed on large zooplankton similar to those collected at the stations (Z2, Z3, and Z5)
within 1 km of a large foraging aggregation of the surface feeders.
These zooplankton include copepods (Calanus hyperboreus),chaetognaths, and ctenophores. These large zooplankton (>5 mg
ind.1) have been frequently observed in the stomach contents ofblack-legged kittiwake and northern fulmar in the fjords of the
Svalbard archipelago, whereas the small zooplankton (<5 mg
ind.1), such as barnacle larvae, did not occur in their diets(Hartley and Fisher, 1936; Mehlum and Gabrielsen, 1993, see also
Urbanski et al., 2017).
Why were large zooplankton more abundant at near surface inthe turbid subglacial meltwater plume? Our small sample of zooplankton supports the previous findings of others; the sedimentrich subglacial discharge that is released at 10–100 m below the

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Figure 3. Density (birds 200 m2) of foraging surface feeders (a) and divers (b) in Bowdoin Fjord in northwestern Greenland. White dots
(smallest dots for black/white version) on each map represent nil. Maps are the natural-colour images taken from satellite on 30 July 2016.

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B. Nishizawa et al.

water surface entrains large volumes of water as it upwells to thesurface, enabling the transport of zooplankton from the depth tothe surface of the fjord (Chu, 2014; Urbanski et al., 2017). This
process supplies abundant zooplankton to the plume surface,where surface feeders can easily access them (Urbanski et al.,2017). Elsewhere, an abrupt drop in salinity to <24 PSU was
found fatal for zooplankton in glacier bays (Zajaczkowski andLegezynska, 2001). Presumably, the zooplankton near the glacierfront is transported from outside of the fjord by the estuarine circulation driven by the glacial meltwater discharge (We˛sławski
et al., 2000). In our study region of Bowdoin Fjord, a clusterednear-surface zooplankton group occurring at the plume in frontof Bowdoin Glacier comprised large amounts of oceanic species,
such as Calanus spp. and chaetognaths, suggesting an inflow fromoceanic water through the bottom of the fjord and upwelling by
plume in front of the glacier (Kanna et al., 2018; Naito et al.,2019). Furthermore, we observed at least 10 black-legged kittiwakes feeding on small fish (probably polar cod) in the plumeaffected section, suggesting that fish are also available at the surface near the glacier front. The fish might be either stunned or
killed by osmotic shock upon entrainment into glacial meltwater.
Polar cod is an important prey (>80% by occurrence and >50%by the total number of prey in stomach samples) of black-legged
kittiwakes feeding in the nearby North Water Polynya, northern
Baffin Bay, during the months of June and July (Karnovsky et al.,2008). A recent study provides photographic and video evidence
of dead redfish and strong upwelling in connection with a tidewater outlet glacier terminating in Godthåbsfjord, west Greenland(Kjeldsen et al., 2014).
High turbidity (>6 FTU) also occurred at stations C36–C38(12–14 km away from the edge of the glacier) in the inside fjord
section (Figure 2c), which might be the result of proglacial
streams from land-terminating glaciers (Kanna et al., 2018). In
this area, few surface feeders and large zooplankton at nearsurface water (at station Z10) were observed (Figures 2a and 3a),presumably because strong upwelling did not occur.

2008, 2011; Frandsen et al., 2014). The accessibility of these preyspecies might be affected by water clarity that regulates the foraging efficiency in visually hunting aquatic seabirds (Ainley, 1977;
Haney and Stone, 1988; Day et al., 2003; Henkel, 2006). Indeed,
the little auks inhabiting the shelf of West Spitsbergen preferred
the areas where C. glacialis was abundant and was clearly visible(Stempniewicz et al., 2013). Little auks dive to a depth of 30 m
to feed mainly on Calanus copepods (Karnovsky et al., 2011;
Brown et al., 2012). We have no information on the density ofthe prey existing at the depth of 30 m in Bowdoin Fjord.
However, the Calanus copepods (C. hyperboreus, C. glacialis, andC. finmarchicus) occurred in the near-surface waters around themouth of fjord (Z12 and Z13) and in the outside fjord section(Z14 and Z15), suggesting that these Calanus copepods might beavailable for little auks at their foraging depth. Water masses in
the outside fjord section showed the highest salinity (28 PSU)
and the lowest turbidity (1.2 FTU), indicating under the influences of the oceanic West Greenland currents. A previous study
conducted in Svalbard’s glacial fjords showed that the density ofsmall copepods, such as Pseudocalanus and Oithona similis, washigh in the inner fjord, whereas the larger copepods, such as
Calanus spp., were abundant in the outer fjords under the influence of oceanic Atlantic water (Walkusz et al., 2009).
In conclusion, our study showed that surface feeders and divers are segregated in space in a glacial fjord and turbidity of glacial meltwater may explain these differences. Importance ofglacial meltwater on seabird habitats has been widely reported
from other areas outside Greenland, including Alaska, Canada,
Russia, and Antarctic (e.g. McLaren and Renaud, 1982; Smithet al., 2007; Arimitsu et al., 2012; Grémillet et al., 2015).
Therefore, careful attention should be paid to the seabird species,
which are the marine top predators, while investigating the impact of changes in tidewater glaciers on the fjord ecosystems.

Supplementary data
Supplementary material is available at the ICESJMS online version of the manuscript.

Foraging habitat of divers
Divers, including the little auk, thick-billed murre, and black guillemot, foraged primarily in the areas outside of the fjord, whereturbidity was the lowest. The little auks, a pursuit-diving species,
feed mainly on energy-rich copepods (Calanus glacialis and C.
hyperboreus) in the oceanic water of the Arctic (Karnovsky et al.,Acknowledgements
We thank Dr Y. Fukamachi, T. Oshima, and K. Peterson who
helped our field observations. We also thank Dr. George Hunt
who provided useful comments on the manuscript. This research
was funded by MEXT (Japanese Ministry of Education, Culture,

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Figure 4. Results of GAM regression for the density of foraging surface feeders (a) and divers (b) as a function of turbidity. Dashed lines are
95% conﬁdence limits. Signiﬁcance levels (p-values) are shown on each plot. Thick marks on the x-axis show the locations of data points.

Contrasting assemblages of seabirds
Sports, Science and Technology) through the Arctic research
project Arctic Challenge for Sustainability (ArCS).

Funding
This research was funded by MEXT (Japanese Ministry of
Education, Culture, Sports, Science and Technology) through the
Arctic research project Arctic Challenge for Sustainability (ArCS).

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