Arctic sea ice a major determinant in Mandt's black guillemot movement and distribution during non-breeding season

Abstract

Mandt's black guillemot (Cepphus grylle mandtii) is one of the few seabirds associated in all seasons with Arctic sea ice, a habitat that is changing rapidly. Recent decreases in summer ice have reduced breeding success and colony size of this species in Arctic Alaska. Little is known about the species' movements and distribution during the nine month non-breeding period (September–May), when changes in sea ice extent and composition are also occurring and predicted to continue. To examine bird movements and the seasonal role of sea ice to non-breeding Mandt's black guillemots, we deployed and recovered (n = 45) geolocators on individuals at a breeding colony in Arctic Alaska during 2011–2015. Black guillemots moved north to the marginal ice zone (MIZ) in the Beaufort and Chukchi seas immediately after breeding, moved south to the Bering Sea during freeze-up in December, and wintered in the Bering Sea January–April. Most birds occupied the MIZ in regions averaging 30–60% sea ice concentration, with little seasonal variation. Birds regularly roosted on ice in all seasons averaging 5 h d−1, primarily at night. By using the MIZ, with its roosting opportunities and associated prey, black guillemots can remain in the Arctic during winter when littoral waters are completely covered by ice.

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Research
Cite this article: Divoky GJ, Douglas DC,
Stenhouse IJ. 2016 Arctic sea ice a major
determinant in Mandt’s black guillemot
movement and distribution during
non-breeding season. Biol. Lett. 12: 20160275.
http://dx.doi.org/10.1098/rsbl.2016.0275
Received: 4 April 2016
Accepted: 17 August 2016
Subject Areas:
ecology
Keywords:
seabird, Arctic, sea ice, black guillemot,
geolocation
Author for correspondence:
G. J. Divoky
e-mail: divoky@cooperisland.org
One contribution to the special feature ‘Effects
of sea ice on Arctic biota’.
Electronic supplementary material is available
online at https://dx.doi.org/10.6084/m9.fig-
share.c.3457497.
Marine biology
Arctic sea ice a major determinant in
Mandt’s black guillemot movement and
distribution during non-breeding season
G. J. Divoky1, D. C. Douglas2and I. J. Stenhouse3
1
Friends of Cooper Island, 652 32nd Avenue E, Seattle, WA 98112, USA
2
US Geological Survey Alaska Science Center, 250 Egan Drive, Juneau, AK, USA
3
Biodiversity Research Institute, 276 Canco Road, Portland, ME 04103, USA
GJD, 0000-0001-9902-8203; DCD, 0000-0003-0186-1104; IJS, 0000-0003-3614-9862
Mandt’s black guillemot (Cepphus grylle mandtii) is one of the few seabirds
associated in all seasons with Arctic sea ice, a habitat that is changing
rapidly. Recent decreases in summer ice have reduced breeding success
and colony size of this species in Arctic Alaska. Little is known about the
species’ movements and distribution during the nine month non-breeding
period (September–May), when changes in sea ice extent and composition
are also occurring and predicted to continue. To examine bird movements
and the seasonal role of sea ice to non-breeding Mandt’s black guillemots,
we deployed and recovered (n¼45) geolocators on individuals at a breeding
colony in Arctic Alaska during 2011–2015. Black guillemots moved north to
the marginal ice zone (MIZ) in the Beaufort and Chukchi seas immediately
after breeding, moved south to the Bering Sea during freeze-up in December,
and wintered in the Bering Sea January– April. Most birds occupied the MIZ
in regions averaging 30– 60% sea ice concentration, with little seasonal
variation. Birds regularly roosted on ice in all seasons averaging 5 h d
21
, pri-
marily at night. By using the MIZ, with its roosting opportunities and
associated prey, black guillemots can remain in the Arctic during winter
when littoral waters are completely covered by ice.
1. Introduction
While the Arctic supports a large and diverse marine avifauna in summer, most
seabirds migrate south in autumn as several million square kilometres of sea ice
growth reduces the amount of ocean available for foraging in winter. Only two
seabird species have their migrations and winter distributions determined by the
formation and presence of Arctic sea ice, the high Arctic populations of black
guillemot (Cepphus grylle) and the ivory gull (Pagophila eburnea) [1]. Black guille-
mots in the western Arctic are in the subspecies mandtii [2], thought to have
occupied a high Arctic refugium in the last glacial maximum [3] with geographi-
cal variation in the mitochondrial DNA of our study population on Cooper
Island reinforcing that view [4]. Black guillemots are pursuit diving piscivores
that in the Beaufort and Chukchi seas prey heavily on Arctic cod (Boreogadus
saida) [5–7], the primary fish species associated with Arctic sea ice [8]. Black guil-
lemots have been observed in the Alaskan Arctic at the ice edge during autumn
[6], and as far north as Pt. Barrow [9] and as far south as the ice edge in the Bering
Sea [10] during winter, but nothing has been documented about non-breeding
habitat use, movements and regional distributions.
Arctic sea ice has been decreasing significantly in recent decades with com-
plete loss in summer possible for mid-century [11], so it is important to
document use of sea ice by one of the few Arctic avian ‘sea ice obligates’. To
this end, we deployed light-sensitive geolocators and data loggers on breeding
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black guillemots at the Cooper Island colony to extend our
knowledge of the subspecies during the non-breeding period.
2. Material and methods
Geolocators were deployed and retrieved at Cooper Island,
Alaska (718200N, 1558410W, figure 1). Breeding black guillemots
were fitted with 1 g geolocators near the end of four breeding
seasons, 2011–2014, and retrieved the following year. We used
British Antarctic Survey (Cambridge, UK) units (Mk13 or Mk14)
in 2011–2012 and Migrate Technology (Cambridge, UK) units
(C-65) in 2013–2014. We attached the geolocator to a plastic leg
band on the bird’s tarsus with a cable tie. The number of geoloca-
tors deployed annually were 6, 9, 26 and 18; with 5, 7, 23 and 10
retrievals, respectively.
We derived noon and midnight positions based on sunset and
sunrise times estimated from light intensity levels that were
sampled every 60 s with maximums stored every 5 min. We
used INTIPROC software (Migrate Technology) to estimate latitude,
based on day length and longitude, based on time of midday
with respect to GMT. Black guillemots sometimes roosted on sea
ice near the time of sunrise and sunset, obscuring the light
sensor and preventing reasonable position estimates. We excluded
estimates before 16 October and between 1 March and 15 April,
because latitudes are unreliable around the vernal and autumnal
equinoxes, and after 1 May, because birds were moving northward
into areas with near 24 h of daylight. After exclusions, we used
1334, 1855, 4993 and 2564 position estimates for analysis of the
four non-breeding periods, respectively.
We used the kernelkcbase function in the R library adehabi-
tatHR [12] with a 150 km smoothing parameter to generate
twice-monthly utilization distributions (UDs) on a fixed 50 km
resolution grid. Twice-monthly UDs were computed with all
years pooled, and for individual years. We used the pooled
UDs to map generalized movements, and the year-specific UDs
to calculate average sea ice concentration [13] within 50% UD
contours during the period of occupancy and +one month.
We used wet/dry logs from Migrate Technology geolocators to
investigate time spent out of water, diurnally and seasonally. Black
guillemots in the western Arctic are regularly seen roosting on sea
ice (G. Divoky 2016, personal observation), and we believe dry
state to be primarily indicative of roosting although an unknown
portion of thedry hours may be of a bird tucking its tarsus and geo-
locator into its plumagewhile in the water, as has been observed for
other alcids [14]. Loggers interrogated wet/drystate every 30 s and
stored cumulative wet-counts every 4 h. We assumed wet/drystate
reflected a 30 s period and computed time dry for each 4 h logging
period. To examine diurnal variation in time dry, we used mid-time
of each 4 h logging period to bin data into four 6 h diurnal periods,
starting at 03.00, 09.00, 15.00, 21.00 local time (GMT-10 h). We also
partitioned data at monthly scales to examine seasonal variations:
post-breeding in the Beaufort and Chukchi seas during Septem-
ber– November, movements to the Bering Sea during December,
winter in the Bering Sea during January–March, and initial
spring migration during April.
3. Results
(a) Distribution and movements
Black guillemots fitted with geolocators completed breeding
between 22 August and 5 September. Although no reliable
geolocator locations were obtained until 16 October, sea sur-
face temperature (SST) and wet/dry state in early September
indicated birds moved north to the sea ice after departing the
breeding colony. The Cooper Island black guillemots
undergo a full-body moult immediately after breeding,
usually completed by late September off northern Alaska
[6], with movements prevented or impaired during flight
feather replacement. Post-breeding movements were primar-
ily northward with the majority of black guillemots between
728and 758N in late October with some individuals possibly
as far north as 778N.
Westward movement into the Chukchi Sea did not occur
until late November as ice covered the Beaufort Sea. Most
birds moved into the Bering Sea from late November to late
December as the Chukchi Sea became ice-covered. From
Figure 1. Pooled locations (dots) of adult Mandt’s black guillemots (n¼45) in twice-monthly periods during four non-breeding seasons (2011–2015) with
average sea ice concentration during the same periods. Polygons depict 90% (thin) and 50% (thick) utilization distributions. Birds were tagged with geolocators
at their Cooper Island breeding colony near Barrow, Alaska.
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January through to April, black guillemots broadly occupied
the partially ice-covered Bering Sea shelf, although a few
individuals returned to the Arctic Basin in February in
some years. Most birds remained in the Bering Sea through
late April, when sea ice was rapidly melting and retreating.
A directed migration northward out of the Bering Sea
occurred in late April and early May when large numbers
of black guillemots begin to stage in open water leads off
Pt. Barrow before returning to Cooper Island in early June
(C. George 2015, personal communication.).
(b) Ice habitat
Black guillemots occupied sea ice habitat in the marginal ice
zone (MIZ) during the entire non-breeding period (figure 2).
While sea ice was forming during October to late February,
birds consistently occupied broad areas where the mean ice
concentration was 43% (s.d. 9.8), averaging 20% more than
a month earlier and 20% less than a month later. In April,
with sea ice melting and retreating, this pattern reversed
and birds continued to occupy regions with similar ice con-
centrations by moving north into areas that earlier had had
more ice. SST data loggers in the 2013 and 2014 deployments
showed birds moved from relatively warm waters (more than
38C) near the colony to waters averaging less than 18C (i.e.
near sea ice) for the remainder of the non-breeding period.
(c) Behaviour
Black guillemots averaged over 5 h per day out of water
throughout the non-breeding period (table 1). Most time
out of water involved night-time roosting on sea ice, with
an average of 3.8 h dry from 21.00 to 09.00 (GMT-10 h), and
less than 1 h from 09.00 to 15.00. Seasonal variation was
low with the exception of January– March in the Bering Sea
when birds spent almost 1.5 h more out of the water than
the other three seasonal periods.
4. Discussion
Our study provides, to our knowledge, the first detailed infor-
mation on movements and habitat use of one of the Northern
Hemisphere’s most northerly wintering seabirds and a truly
pagophilic population adapted to occupyArctic sea ice habitats
p
eriod
100
80
60
40
20
0
late
Oct Nov Dec Jan Feb Apr
lateearly late late lateearly early early late
ice concentration (%)
Beaufort
Chukchi Chukchi Chukchi
Bering Bering
occupancy
one month pre-occupancy
one month post-occupancy
Figure 2. Average sea ice concentration (+1 s.d.) within annual (n¼4 years) twice-monthly 50% utilization distributions (UDs) of Mandt’s black guillemots
(blue), and within the same UDs one month before (green) and one month after (red) occupancy.
Table 1. Mean hours per day Mandt’s black guillemots spend out of water, diurnally and seasonally, during the non-breeding period.
03.00–09.00 09.00 – 15.00 15.00 – 21.00 21.00–03.00
hours dryperiod location mean s.d. mean s.d. mean s.d. mean s.d.
Sep–Nov Beaufort/Chukchi 1.35 1.56 0.55 0.68 1.37 1.51 1.72 1.86 4.99
Dec Chukchi/Bering 1.72 2.01 0.52 0.69 1.05 1.48 1.73 2.04 5.02
Jan–Mar Bering 2.38 2.18 0.47 0.65 1.04 1.35 2.58 2.38 6.47
Apr Bering 1.28 1.56 0.74 0.90 1.32 1.46 1.79 1.88 5.14
Sep–Apr 1.78 1.94 0.54 0.71 1.20 1.45 2.05 2.13 5.14
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throughout the year. Most members of the genus Cepphus inha-
bit near shore littoral waters in breeding and non-breeding
seasons [15], where they use a prey base that is more predict-
able, less patchy and at shallower depths, while maintaining
access to coastal roosting sites. In regions where the littoral
zone is ice-covered for much of the year, pelagic sea ice offers
a proxy to coastal habitat by providing sympagic fauna and a
roosting substrate. Mandt’s black guillemot probably became
adapted to sea ice habitats when restricted to an unglaciated but
ice-covered refugium in the Arctic during the last glacial maxi-
mum [4], and the observations presented here demonstrate a
continued association with that habitat.
The physical and biological changes associated with sea
ice formation and melt are the primary factors influencing
black guillemot movements in the western Arctic. Migration
in the non-breeding period was primarily facultative, being
correlated with the advancement of sea ice. Interannual move-
ments responded to short-term variations (i.e. +two weeks) in
sea ice distribution that were averaged in figure 1. While unpre-
dictable annual and seasonal variation in prey availability is
the primary stimulus for most facultative movements in birds
[16], the southward movements appeared not to be limited
solely to prey but in response to the southward shift of the
MIZ. Movement related to suitable sea ice habitat and not
necessarily prey has been recorded in Antarctic seabirds [17].
It is not known if Arctic cod also move with the advancing
ice. Black guillemots prey on Arctic cod at the advancing ice
edge in autumn [6,18], and the size and depth of Arctic cod
in the Bering are suitable for black guillemots [19]. While
Arctic cod or alternative prey may be most available at the
ice concentrations favoured by black guillemots in the MIZ,
benefits offered by physical ice characteristics may play an
important role in habitat preferences. Because black guillemots
spend approximately 20% of the day roosting on sea ice, birds
may be selecting areas with appropriate ice thickness and con-
centration for roosting. The benefits of roosting versus sitting
on the water are negatively correlated with water tempera-
ture, so ice suitable for roosting would be essential when
occupying the freezing winter waters of the Bering Sea, as it
is for spectacled eiders (Somateria fischeri) wintering there [20].
Conditions south of preferred ice may be less optimal for
roosting, foraging and protection from storms owing to an
abundance of thin frazil ice in low concentrations or compe-
tition from seabird species less adapted to sea ice. The
observed departure from areas of increasing ice concentration
could be in response to decreased foraging opportunities in
heavy ice, or to increased risks of occupying areas where
open water could rapidly disappear from wind-driven compac-
tion or sudden freezing, which is known to be a source of
mortality for wintering black guillemots [21]. While most indi-
viduals occupied the MIZ, it is important to note that once ice
formation was nearly complete in February, birds broadly occu-
pied much of the Bering/Chukchi shelf with some positioned
southerly, whereas others had returned to the Arctic Basin.
Recent losses in summer sea ice have impacted black
guillemot breeding success on Cooper Island, owing to
diminished accessibility to Arctic cod, but annual adult survi-
val has shown no trend over the past four decades [7]
indicating no decadal trend in prey availability in the MIZ.
Future changes in Arctic sea ice can be expected to cause
major alterations in the distribution and timing of Mandt’s
black guillemot movements and distribution as summer ice
is predicted to disappear and winter ice to greatly decrease
in this century [22,23].
Ethics. Animal handling protocols were approved by US Geological
Survey (bird banding permit no. 21675).
Data accessibility. Location and wet/dry sensor data are available in the
electronic supplementary material.
Authors’ contributions. G.J.D. conceived the study assisted by I.J.S. G.J.D.
conducted the fieldwork. G.J.D. and D.C.D. performed analyses. All
authors wrote the manuscript, approved the final version, and agree
to be held accountable for the manuscript’s contents.
Competing interests. We have no competing interests.
Funding. Support for fieldwork and analyses (G.J.D.) were provided by
the non-profit organization Friends of Cooper Island.
Acknowledgements. We thank the Biodiversity Research Institute for pro-
viding geolocators in 2011 to initiate the study, the North Slope
Borough’s Department of Wildlife Management for logistical support
of fieldwork on Cooper Island, and Penelope Chilton for assisting
with fieldwork and data processing. Any use of trade, firm, or pro-
duct names is for descriptive purposes only and does not imply
endorsement by the US Government.
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