Responding to climate change: Adélie Penguins confront astronomical and ocean boundaries.

Abstract

Long-distance migration enables many organisms to take advantage of lucrative breeding and feeding opportunities during summer at high latitudes and then to move to lower, more temperate latitudes for the remainder of the year. The latitudinal range of the Adélie Penguin (Pygoscelis adeliae) spans approximately 22 degrees. Penguins from northern colonies may not migrate, but due to the high latitude of Ross Island colonies, these penguins almost certainly undertake the longest migrations for the species. Previous work has suggested that Adélies require both pack ice and some ambient light at all times of year. Over a three-year period, which included winters of both extensive and reduced sea ice, we investigated characteristics of migratory routes and wintering locations of Adélie Penguins from two colonies of very different size on Ross Island, Ross Sea, the southernmost colonies for any penguin. We acquired data from 3-16 geolocation sensor tags (GLS) affixed to penguins each year at both Cape Royds and Cape Crozier in 2003-2005. Migrations averaged 12760 km, with the longest being 17 600 km, and were in part facilitated by pack ice movement. Trip distances varied annually, but not by colony. Penguins rarely traveled north of the main sea-ice pack, and used areas with high sea-ice concentration, ranging from 75% to 85%, about 500 km inward from the ice edge. They also used locations where there was some twilight (2-7 h with sun < 6 degrees below the horizon). We report the present Adélie Penguin migration pattern and conjecture on how it probably has changed over the past approximately 12000 years, as the West Antarctic Ice Sheet withdrew southward across the Ross Sea, a situation that no other Adélie Penguin population has had to confront. As sea ice extent in the Ross Sea sector decreases in the near future, as predicted by climate models, we can expect further changes in the migration patterns of the Ross Sea penguins.

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Ecology, 91(7), 2010, pp. 2056–2069
? 2010 by the Ecological Society of America
Responding to climate change: Ade ´lie Penguins confront
astronomical and ocean boundaries
GRANT BALLARD,1,2,7VIOLA TONIOLO,3DAVID G. AINLEY,4CLAIRE L. PARKINSON,5KEVIN R. ARRIGO,3
AND PHIL N. TRATHAN6
1PRBO (Point Reyes Bird Observatory) Conservation Science, 3820 Cypress Drive #11, Petaluma, California 94954 USA
2Ecology, Evolution, and Behaviour, School of Biological Sciences, University of Auckland, Auckland, New Zealand
3Department of Environmental Earth System Science, Ocean Biogeochemistry Lab, Stanford University,
Stanford, California 94305-2215 USA
4HT Harvey & Associates, 3150 Almaden Expressway, Suite 145, San Jose, California 95118 USA
5Cryospheric Sciences Branch, NASA/Goddard Space Flight Center, Greenbelt, Maryland 20771 USA
6British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road,
Cambridge CB30ET United Kingdom
Abstract.
lucrative breeding and feeding opportunities during summer at high latitudes and then to
move to lower, more temperate latitudes for the remainder of the year. The latitudinal range of
the Ade ´ lie Penguin (Pygoscelis adeliae) spans ;228. Penguins from northern colonies may not
migrate, but due to the high latitude of Ross Island colonies, these penguins almost certainly
undertake the longest migrations for the species. Previous work has suggested that Ade ´ lies
require both pack ice and some ambient light at all times of year. Over a three-year period,
which included winters of both extensive and reduced sea ice, we investigated characteristics of
migratory routes and wintering locations of Ade ´ lie Penguins from two colonies of very
different size on Ross Island, Ross Sea, the southernmost colonies for any penguin. We
acquired data from 3–16 geolocation sensor tags (GLS) affixed to penguins each year at both
Cape Royds and Cape Crozier in 2003–2005. Migrations averaged 12760 km, with the longest
being 17600 km, and were in part facilitated by pack ice movement. Trip distances varied
annually, but not by colony. Penguins rarely traveled north of the main sea-ice pack, and used
areas with high sea-ice concentration, ranging from 75% to 85%, about 500 km inward from
the ice edge. They also used locations where there was some twilight (2–7 h with sun ,68 below
the horizon). We report the present Ade ´ lie Penguin migration pattern and conjecture on how it
probably has changed over the past ;12000 years, as the West Antarctic Ice Sheet withdrew
southward across the Ross Sea, a situation that no other Ade ´ lie Penguin population has had
to confront. As sea ice extent in the Ross Sea sector decreases in the near future, as predicted
by climate models, we can expect further changes in the migration patterns of the Ross Sea
penguins.
Long-distance migration enables many organisms to take advantage of
Key words:
adeliae; Ross Sea; sea ice; wintering ecology.
Ade´lie Penguin; Antarctica; climate change; geolocation sensor; migration; Pygoscelis
INTRODUCTION
Long-distance migration enables many organisms to
take advantage of lucrative breeding and feeding
opportunities during summer at high latitudes and then
to move to lower, more temperate latitudes for the
remainder of the year (cf. Cockell et al. 2000, Alerstam
et al. 2003), a situation complicated for northern
terrestrial species in the past million years by the ebb
and flow of continental ice sheets (Greenberg and Marra
2005). Marine species that undertake polar-temperate
long-distance migrations include seabirds (e.g., Phillips
et al. 2005), seals (e.g., McConnell and Fedak 1996), and
whales (e.g., Clapham and Mattila 1990), but the history
of change in their migration has been little investigated.
The glaciological history of Antarctica, however, has
been intensively studied. Because of the unique cold and
dry conditions, which preserve subfossil deposits, the
appearance and disappearance of Ade ´ lie Penguin
(Pygoscelis adeliae) colonies, as glaciers and sea ice
have come and gone, is well understood (Emslie et al.
1998, 2003, 2007; see also Thatje et al. 2008). What we
know little of, however, is how the penguins respond in
real time to the seasonal flux in sea ice, an important
detail in understanding the Holocene history of this
species. Environmental changes now occurring, espe-
cially in the winter, are affecting seabird numbers and
demography (Barbraud and Weimerskirch 2003). Of
particular interest is how Antarctic seabirds cope with
two challenges: variability in the location of their
Manuscript received 22 April 2009; revised 15 September
2009; accepted 13 October 2009. Corresponding Editor: J. P. Y.
Arnould.
7E-mail: gballard@prbo.org
2056

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foraging habitat (the sea ice ecosystem) and in the
amount of light available to them for foraging and
navigating.
The Ade ´ lie Penguin is one of the southernmost
breeding birds in the world, its overall breeding range
extending over ;228 of latitude (56–788 S; Woehler
1993). Ade ´ lies are pack-ice obligates while at sea (Ainley
et al. 1983, 1984, 1994), previously documented as
preferring about 70% ice cover (Cline et al. 1969).
Southern Ade ´ lies are known to depart their breeding
grounds in February, thus avoiding a long, dark, ice-
covered, and extremely cold winter. In the northern
portion of their range, penguins visit colonies year
round (Parmelee et al. 1977). Only in those northern
areas have the species’ winter movements previously
been investigated (Fraser and Trivelpiece 1996, Clarke et
al. 2003).
In the southernmost part of this species’ range, its
habitat has been in constant flux through recent
millennia and likely will remain so into the near future.
The West Antarctic Ice Sheet (WAIS) withdrew
southward across the Ross Sea to its present position
only since the time of the first Egyptian pharaohs
(;6000 yr BP; Emslie et al. 2003, 2007). As it withdrew,
new breeding habitat was sequentially exposed from 728
S (northern portion of the Ross Sea) during the Last
Glacial Maximum (LGM) to almost 788 S at present
(Ainley 2002). Although the ocean was productive in the
outermost Ross Sea during the LGM (Thatje et al.
2008), as it is now throughout (Arrigo et al. 1998, 2008),
only by migrating could Ade ´ lies take advantage of the
new breeding opportunities. Providing a challenge,
though, are the shortening duration of favorable climate
conditions for breeding with increasingly higher latitude,
as well as the shortening amount of daylight, since
Ade ´ lies are visual predators (Wilson et al. 1993) and
require daylight for navigation (Emlen and Penney 1964,
Penney and Emlen 1967). The southern Ross Sea is well
south of the Antarctic Circle and, therefore, dark during
half of the year. On the other hand, the seasonal
schedule of sea ice advance, extent, and retreat is
changing noticeably (Parkinson 2002, Zwally et al.
2002, Stammerjohn et al. 2008, Turner et al. 2009), a
critical development for this ice-obligate species (Emslie
et al. 1998). Investigating the migratory strategy of
Ade ´ lie Penguins can therefore reveal insights into how
they have met the challenges of receding and otherwise
changing ice sheets, as well as into how they are likely to
respond to future changes in their sea ice environment
(Ainley et al. 2010).
Here we report results of the first use of GLS
(geolocation sensor) tags to track the year-round
movements of Ade ´ lie Penguins. We sought to document
the general pattern (distance, direction, speed, location)
of movement, and we hypothesized that Ade ´ lies select
wintering locations based on two criteria: (1) sea ice
present but not so consolidated as to prevent access to
the ocean, and (2) light sufficient to see well enough to
forage. We believe that these two factors are important
in the evolution of migratory patterns in this species (see
Fraser and Trivelpiece 1996). We also predicted that
penguins originating from two different colonies, Capes
Royds and Crozier, would use different wintering
locations, with potentially different arrival times and
ice and light characteristics, because onset of breeding
(as well as autumn departure) differs by as much as a
week and population trends at these two colonies have
followed disparate trajectories, with over-winter survival
being an important determinant of population trends
(Ainley et al. 1983, Trathan et al. 1996, Wilson et al.
2001). Annual survival rates at the smaller colony (Cape
Royds; 2500 pairs) appear to be consistently lower than
those at the larger colony (Cape Crozier; 150000 pairs)
(K. Dugger, D. Ainley, and G. Ballard, unpublished
data).
MATERIALS AND METHODS
At the end of the Ade ´ lie Penguin breeding seasons
(end of January) of 2003/2004, 2004/2005, and 2005/
2006, we attached GLS tags to 10–20 penguins at each
of two colonies on Ross Island: Cape Crozier and Cape
Royds (98 total tags, 41 retrieved functioning; Table 1;
see also Appendix A). We chose these two colonies
because they are markedly different in size, which has
implications for several aspects of this species’ breeding
biology (Ainley et al. 2004). Moreover, the penguins at
Royds nest 7–10 d later than those at Crozier and thus
have a different annual phenology.
We selected only birds that were feeding large, cre ` ched
chicks and appeared in good physical condition in late
January and early February. We did this to increase the
probability that we would be able to find these birds the
following spring, at which time we caught them again to
remove the archival tags. Birds were sexed by cloacal
exam (at Crozier) in 2003 and by size, behavior, and
timing of colony attendance in all other years and
TABLE 1.
Ade ´ lie Penguins (Pygoscelis adeliae) from the Cape Crozier and Cape Royds colonies, Ross Island, Antarctica.
Winter locations (June–July), arrival date, hours of twilight, distance to pack ice edge, and pack ice concentration for
YearnLatitudeLongitude
Arrival date
(week of year)
Twilight
hours
Distance to
pack ice edge (km)
Ice concentration
(%)
2003
2004
2005
11 (77)
13 (78)
17 (98)
?66.54 6 0.57
?68.52 6 0.41
?69.96 6 0.59
180.43 6 2.90
177.76 6 3.32
185.44 6 2.38
23.0 6 0.0
25.3 6 0.4
24.5 6 0.3
6.14 6 0.11
5.20 6 0.11
4.11 6 0.20
341.66 6 24.56
525.12 6 16.26
631.13 6 22.57
74.12 6 2.37
81.13 6 0.68
81.56 6 0.55
Notes: Sample sizes (n) are the number of individuals, with number of positions in parentheses. Values are means 6 SE.
July 20102057PENGUIN MIGRATION AND CLIMATE CHANGE

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locations (Ainley and Emison 1972, Ainley et al. 1983,
Kerry et al. 1992).
Encased within the epoxy block of each 9-g GLS tag
(MK3 tag; Afanasyev 2004) were a battery (rated for a
3-yr life), a light sensor, a clock, and a microchip for
data storage. Each device was fastened to a white Darvic
plastic band (A. C. Hughes, Middlesex, UK) using a
Panduit stainless steel cable tie (Panduit, Tinley Park,
Illinois, USA). The plastic band (with tag attached) was
placed on the left leg of the penguins. We chose a white
band to match the color of the leg feathers because
penguins will attempt to remove anything affixed to
them that is any color other than black or white (Wilson
and Wilson 1989). This method of attachment required
,5 min of handling per individual.
The nests of tagged birds were flagged, with positions
recorded by GPS in order to facilitate tag retrieval. We
searched for individuals with tags each spring by
frequently scanning all birds within 5–10 m of nest
markers. Tags were removed upon detection; all data
pertaining to the bird’s breeding status and condition
were recorded if they could be determined, and the tag’s
archives were immediately downloaded. When recap-
tured, most birds were breeding, and had minimal
feather wear around the tag area and some callusing on
the leg. Five individuals had more severe callusing, and
one individual limped prior to tag removal, we think
because the band was attached too loosely (the bird
subsequently recovered completely). Tag attrition was a
function of normal over-winter penguin mortality
(estimated range 4–27% annual mortality for 1996–
2002 at Cape Crozier; Dugger et al. 2006), tag loss, tag
and band loss or tag malfunction. It is also possible that
the tags increased adult mortality, although we have no
direct evidence of this. We retrieved 65% of the tags
within one year, and 68% after two or more years (data
from these tags not reported in this study). We believe
that some individuals were missed because GLS tags
were inconspicuous and emigration rates were higher
than normal (Shepherd et al. 2005); at least two birds
were missed for one year and one bird, from Royds, for
two years, where temporary emigration owing to a large
grounded iceberg was especially high (K. Dugger, D.
Ainley, P. Lyver, K. Barton, and G. Ballard, unpublished
data). Annual variability in survival and effects of
marking penguins remain under study (Dugger et al.
2006; K. Dugger, D. Ainley, and G. Ballard, unpublished
data).
Light data collected by GLS tags were analyzed using
MultiTrace software (Jensen Software Systems, Laboe,
Germany). The GLS tags measured visible light every 60
s and recorded the maximum reading every 10 min. By
recording light level, day length could be estimated for
each day of deployment. The midpoint of a local day
(light period) was taken as noon; the midpoint of a local
night (dark period) was taken as midnight. The local
time of noon and midnight were compared against
GMT (Greenwich Mean Time) to determine longitude;
day length on a given date was used to determine
latitude (Hill 1994).
Fast-moving animals may cover large distances in an
east–west direction during a 24-h period. Under such
scenarios, the calculated day length may be more or less
than 24 h and calculations of latitude must be
compensated accordingly. This correction factor enables
the compensation algorithm to take into account
whether travel occurred mainly during the day or night.
Penguins travel relatively slowly (compared with flying
birds, for example), and in the absence of any evidence
to suggest otherwise, we applied the default correction
factor of 0.5 (i.e., equally likely to travel during light or
dark). Given the inaccuracy of latitude estimation
during equinoxes (Hill 1994), we excluded the period
around the equinoxes when location estimates were
clearly affected (;1 week before and 3 weeks after the
autumnal equinox, 3 weeks before and 2 weeks after the
vernal equinox). Any locations derived from light curves
with obvious interruptions or interference around the
times of sunset or sunrise (probably as a result of diving
or of changes in orientation, or intermittent shading of
the sensor by snow, ice, or feathers) were noted during
processing and subsequently excluded if obviously
anomalous (Hill 1994).
To reduce the position error inherent in GLS data
(Phillips et al. 2004), penguin positions (two per day,
one at noon and one at midnight) were smoothed using
a 5-day moving average weighted by location and
number of neighbors. We chose this 5-day period
because we felt that fewer days resulted in overconfi-
dence of positions and more than 5 days underutilized
the detail available in the data. Weekly means of these
positions for each individual were used for all analyses.
Data were filtered to remove any locations that
required unrealistic swim speeds between estimated
positions (.2.3 m/s sustained over a 12-h period; Clark
and Bemis 1979, Brown 1987). The great-circle distance
between consecutive fixes was used in all velocity
calculations. We were unable to obtain any positions
until the time of first sunset, which in the southern Ross
Sea is 20 February, by which time all penguins had
already departed Ross Island.
We deployed three static GLS tags to overwinter at
Cape Crozier (778 S) and three at Cape Hallett (728 S) in
2004, to be used as a reference. These data were
processed as just outlined, and results were compared
with device locations determined precisely by GPS.
Potential consistency in errors (great-circle distances)
among devices and among days was examined, with
midday fixes only used in the comparisons to reduce the
problem of lack of serial independence. Results from the
analyses of the static devices were used to help
parameterize some of the inputs to MultiTrace and to
verify the importance of eliminating data near the
equinoxes, as described previously.
To assess the overall validity of the positions that we
report for penguins, we analyzed the known error in the
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data from static devices after processing these data in the
same way we had processed the data from tags deployed
on penguins. Thus, the position data from the Cape
Hallett reference devices were evaluated to estimate
mean error in penguin data using a mixed-effects model
with tag identification included as a random effect and
week as a main effect. We chose to use only Cape Hallett
data for this analysis because its latitude more closely
approximated the average positions of the penguins in
the analysis. Results of these analyses showed that
weekly mean errors (6SE) were lowest in June and July
(33.0 6 0.3 km) and highest in February and October
(99.2 6 0.4 km). The overall mean error was estimated
to be 58.6 6 0.8 km. Such accuracy may be surprising
(cf. Phillips et al. 2004), but two factors combine to
explain why this level of accuracy was achieved. First,
error rates are known to be highest near the equinoxes,
and these positions were removed from our data.
Second, the use of a mixed-effects model would smooth
estimates and further reduce error.
To compensate for the gap in GLS data due to the
absence of darkness in the first portion of each
deployment, we also tracked the late-summer (late
January to late February, 2004–2006) movements of
10 individuals using 20–26 g satellite tags (SPOT4 and
SPLASH; Wildlife Computers, Redmond, Washington,
USA; note that these individuals did not also have GLS
tags) affixed to the back feathers of breeders (for
attachment methods, see Wilson and Wilson 1989,
Ballard et al. 2001). Tags were set to transmit every 45
s for the first eight successive transmissions and then
switch to once every 90 s thereafter, with up to 1440
transmissions allowed per day. Tags were programmed
to turn off after being dry for 6 h in order to conserve
batteries. All transmissions were received and processed
within the ARGOS system (CLS Corporation, Ramon-
ville Saint-Agne, France). Data from these tags were
available until the transmitters were lost (due to
molting), died (due to low battery voltage), or stopped
transmitting (after being dry for .6 h and not re-
immersed). Positions with ARGOS accuracy code Z
were deleted, all others (i.e., A, B, 0, 1, 2, 3) were
included only if they were within an appropriate
distance, given penguin swimming speed (,2.3 m/s)
and time between positions from at least two other
locations with code of 1, 2, or 3 (i.e., ?1000 m error),
with no more than 12 h allowed between positions.
We calculated the potential wintering area of Ade ´ lie
Penguins from Ross Island by creating a polygon
containing all GLS-derived penguin positions for all
winters using the following boundaries: the Antarctic
coastline, the eastern and westernmost longitudes, and
the northernmost latitude in the retrieved positions (Fig.
1). Thus, the potential wintering polygon included any
place where a penguin might be found during the
nonbreeding period based on empirical results from this
study. We were not attempting to define the precise area
(e.g., by using kernel analysis) used by penguins. Our
interest was in estimating the area of potential use (for
the study period), and we do not expect that our study
included the full range of possible wintering locations
for these penguins. For each penguin position and for 30
random locations for each week, we calculated the mean
ice concentration within 100 km, the distance to the
large-scale ice edge (as defined by the 15% ice
concentration contour), the number of hours of light
(twilight and daylight), and the distance to the latitude
of 24-h darkness. Weekly time of sunrise and sunset and
civil twilight (sun ,68 below the horizon) for each 150
latitude were obtained from the U.S. Naval Observatory
website (data available online).8
Mean weekly sea ice concentrations and distance to
the large-scale ice edge (as defined by the 15% ice
concentration contour) were derived from the Special
Sensor Microwave Imager (SSM/I) on board the F13
satellite of the Defense Meteorological Satellite Program
(DMSP). Data were collected daily and mapped to a
resolution of 25 3 25 km grid cell size (Cavalieri et al.
2006). Calculation of ice concentration was possible due
to the strong contrast between microwave emissions of
ice and water. Daily ice motion vector data for 2003
were obtained from the website of the Polar Remote
Sensing Group of the Jet Propulsion Laboratory,
California Institute of Technology (available online).9
We created monthly averages of daily ice flow rates and
bearings to evaluate variability in these parameters in
the context of penguin movements in a descriptive sense.
To assess direct effects of ice movement (speed and
direction) on penguin movements, we used weekly mean
values for all grid cells within 100 km of weekly mean
penguin positions. To assess the effect of ice speed on
penguin speed (km/d), we used a mixed-effects general-
ized linear model with penguin identity (ID) included as
a random effect and week of year as a fixed (categorical)
effect, predicting that the effect of ice speed on penguin
speed would vary by week (after removing the 5% of
penguin weekly speeds that were calculated to be .97
km/d, which we assume to be due to location errors).
Separately, we assessed the correlation between ice
movement direction and penguin movement direction
using the circcorr package in STATA (Cox 1998).
Using two-tailed t tests, we compared distance to ice
edge (negative for south, positive for north), mean ice
concentration values, and distance to locations with at
least two hours of twilight per day for actual wintering
positions (n ¼ 253; Table 1) with 30 randomly selected
locations for each week (n ¼ 630) within the potential
wintering area. To inspect the difference in mean ice
concentrations between penguin locations and random
locations, we calculated the univariate kernel density for
each type of location using the Epanechnikov kernel
function (STATA: kdensity).
8hhttp://aa.usno.navy.mil/data/docs/RS_OneDay.phpi
9hhttp://rkwok.jpl.nasa.gov/icemotion/download_MV.htmli
July 2010 2059PENGUIN MIGRATION AND CLIMATE CHANGE

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(Fig. continues on next page)
GRANT BALLARD ET AL.2060 Ecology, Vol. 91, No. 7

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The random locations were assessed so that we could
compare characteristics of places that penguins utilized
with ones that were available to the penguins but not
necessarily occupied. For all analyses of wintering areas,
we used positions from 1 June to 31 July. This period
corresponds to the peak of winter darkness, and the time
for which we had the most consistent position data.
After determining the mean distance from the ice edge
for wintering penguins, we calculated the minimum date
that penguins reached this distance in each year
(necessary only for penguins that did reach this
distance); this was a proxy for ‘‘wintering-area arrival
date.’’ We defined the northward migration period in
days as winter-area arrival date minus 5 February (the
approximate mean departure date; G. Ballard and D.
Ainley, personal observations), and northward migration
speed is the distance from the colony on the winter
arrival date/northward migration period. We used
ANOVA to evaluate effects of colony and year on
northward migration speed.
We calculated the maximum distance that penguins
reached during winter, and the time it took to reach that
point and to return from that point (assuming an
average arrival date of 1 November; G. Ballard and D.
Ainley, personal observation) for each individual in each
year. We used ANOVA to evaluate effects of colony and
year on arrival dates to the maximum wintering
distance, and on average speed sustained to reach and
return from the maximum wintering distance.
FIG. 1.
Appendix A: Fig. A1). Penguin locations are excluded for March and September due to inaccuracy in GLS (geolocation sensor)
positions near equinoxes (see Materials and methods). Sea ice concentration was derived from the Special Sensor Microwave Imager
on board the F13 satellite of the Defense Meteorological Satellite Program. Black is ocean; light colors represent sea ice (lighter¼
higher ice concentration). Orange starbursts are Cape Crozier penguins; blue crosses are Cape Royds penguins as determined by
GLS tags. The average southern boundary of the Antarctic Circumpolar Current is shown near the top of each image (fine dotted
line), along with the Antarctic Circle (more northerly latitude line, bold dotted) and the latitude of zero winter twilight (72.78 S,
lower medium dotted line). The Ross Sea shelf break is indicated with a solid white line (2000-m isobath; Davey 2004), and the
average location of the Balleny Island polynya is indicated with a gray hatched oval (based on combined winter sea-ice data 2003–
2004). The Ross Ice Shelf is at the center of the bottom of each image. Base map layers are from British Antarctic Survey (1998).
Small black squares and polygons are missing sea ice data; white squares and polygons are ‘‘masked’’ during the data processing by
NSIDC (i.e., no ice values were calculated for those cells because of their proximity to land or ice shelves).
Ade ´ lie Penguin locations and sea ice concentration and distribution for February–October 2004 (for 2003–2005 see
July 2010 2061PENGUIN MIGRATION AND CLIMATE CHANGE

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We used mixed-effects general linear models with ID
treated as a random effect to evaluate whether latitude,
longitude, twilight period, distance to ice edge, and sea-
ice concentration varied by colony and year. Twilight
hours were squared and ice concentration values were
arcsine square-root transformed in order for model
residuals to comply with assumptions of normality;
other terms met model assumptions without transfor-
mation. All statistical tests were conducted using
STATA v. 10 (Stata Corporation 2008). We report
means 6 SE throughout.
RESULTS
General migration patterns
At-sea movements.—The migration of most Ade ´ lie
Penguins from Cape Crozier roughly followed a
clockwise course (Fig. 1; see Appendix B), as follows:
(1) in February, birds migrated toward the NNE toward
the nearest residual pack ice (eastern Ross Sea), where
they began molt (Fig. 2); (2) during molt, resting on an
ice floe for 3 weeks, they moved northward and
somewhat westward in a pattern consistent with pack
ice movement (Appendix C); (3) by late fall and early
winter, probably as a result of ice flow, they were located
in the pack ice in the vicinity of the continental shelf
break; (4) subsequently, they moved farther north,
occasionally visiting the Balleny Islands Polynya (an
area of open water in the ice pack) but otherwise
remaining relatively near the large-scale ice edge, which
generally occurs between the Antarctic Circle and the
Antarctic Circumpolar Current (ACC) southern bound-
ary; once out of the Ross Sea they became entrained in
the Ross Gyre (see Jacobs et al. 2002: Fig. 1), which
prevented them from being advected much farther away
from Ross Island (Fig. 1; Appendices B and C); (5) by
late winter they moved with the ice eastward along the
ice edge; and (6) in late September and October they
moved south and then west, returning to their breeding
colonies. The general pattern of movement for penguins
from Cape Royds was north through the various
polynyas along the way, finally reaching the large-scale
ice edge somewhat west of most of the individuals
breeding at Crozier, and then movement east and south
against the flow of ice in the spring (Fig. 1; Appendices
B and C).
Overall, penguin movement speed was correlated with
ice movement speed (b ¼ 5.45 6 1.18 km/d, Z ¼ 4.60, P
, 0.0001; n¼11 individuals, 336 positions). We did not
detect a correlation between penguin and ice movement
direction (r¼0.028, P¼0.76), although the relationship
with speed supports the concept that penguins were
generally moving in the same direction as the ice.
Trip length.—Trip length (including all meanders) for
all years was 12760 6 468.9 km, mean 6 SE (n ¼ 41,
range 8539–17600 km). Trip lengths varied annually
(F2,27¼ 29.65, P , 0.0001), but not by colony (F1,27¼
0.08, P¼0.78). In 2003 penguins made longer trips than
in 2004 and 2005 (P , 0.0001). Maximum great-circle
distance that penguins journeyed from home colonies
averaged 1722 6 66.3 km (n ¼ 41, range 946–2552 km)
and also varied by year (F2,38¼ 4.96; P ¼ 0.01) but not
by colony (F1,38¼ 0.55, P ¼ 0.46).
Traveling speed.—Penguins reached their first winter-
ing locations in mid-to-late June each year (mean date
20 June 6 1.7 d) and reached their maximum distance
from colonies in mid-July to early August (mean date 22
July 6 11.9 d). Penguins traveled more rapidly while
returning from their maximum wintering distance than
they did while reaching this distance (31.71 6 3.73 km/d
[mean 6 SE] vs. 15.09 6 1.99 km/d, respectively; t ¼
?3.93, P ¼ 0.0001). Travel speeds to and from this
distance did not vary by colony or year (for all tests, P .
0.10). Penguins were also faster returning from their
maximum distance than they were arriving at their first
wintering location (10.35 6 0.40 km/d). Penguins
traveled northward to their first wintering locations
more swiftly in 2003 than in 2004 or 2005 (12.34 6 0.60
vs. 9.52 6 0.41 km/d and 9.21 6 0.58 km/d, respectively;
F2,30¼ 11.22; P ¼ 0.0003), but no colony effect was
evident (F1,30¼ 1.42; P ¼ 0.24).
Wintering areas
Overall mean latitude of wintering positions for
Crozier penguins was 68.818 S 6 0.508 (n ¼ 26) and
for Royds penguins was 68.298 S 6 0.598 (n¼15). Mean
longitude for Crozier penguins at 175.298 W 6 1.878 was
quite disparate from that of Royds penguins, 176.448 E
6 2.868 (note the E–W difference). Latitude was
significantly affected by year (Z ¼ ?4.59, P , 0.0001;
Table 1) but not by colony Z¼ 1.31, P ¼0.19), whereas
longitude was significantly affected by colony (Z ¼
?2.76, P ¼ 0.006) but not by year (Z ¼ 1.73, P ¼ 0.08).
Despite the large spatial spread in wintering locations
and the relatively smaller sample size from Cape Royds,
in all years Royds birds wintered west of Crozier birds
(8.278 average difference; Fig. 3).
Arrival week at the first winter location was most
commonly between 11 and 17 June and varied among
years (week 23 in 2003, week 25 in 2004 and 2005; F2,29¼
15.16, P , 0.0001) but not colonies (F1,26¼ 2.88, P ¼
0.10). Arrival date at the maximum distance from the
colony averaged 22 July 6 11.92 d, not consistently
varying among colonies or years (F3,38¼0.56, P¼0.64).
Characteristics of wintering area
Ice extent and concentration.—Ice extent in the
combined potential penguin wintering area varied
annually, with 2003 having the largest extent in
March–June, 2004 being intermediate, and 2005 having
the least (Fig. 1; see Appendix B). Maximum ice extent
was reached earliest in 2003 and latest in 2005. Ice
concentration at random locations in the penguin
wintering area was highest in 2003 (80.9% 6 1.3%)
and lower in 2004 and 2005 (75.0% 6 1.5% and 75.5% 6
1.5%; F2,627¼ 4.87, P ¼ 0.008).
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Ice concentrations where penguins were located were
approximately the same as at random locations, 79.2%
6 0.8 % vs. 77.1% 6 0.86% (P ¼ 0.16). Penguins were
not found in locations with either 100% or 0% ice cover
(Fig. 4). The overall kernel density of penguin location
by ice concentration implies that penguins preferred ice
cover between ;75% and 85%, whereas random
locations reached highest density between 80% and 90%.
We did not detect a difference in ice concentration at
wintering locations by colony (n ¼ 253 positions for 41
individuals, Z¼1.09, P¼0.28) or by year (Z¼1.52, P¼
0.13; Table 1).
Distance to ice edge (15% ice concentration con-
tour).—Penguins almost never ventured north of the
large-scale ice edge (4 of 253 weekly positions ¼ 1.6%),
whereas random points were more often located north
of the edge (i.e., in open water; 31 of 630 positions ¼
4.9%). Among positions north of the ice edge, penguins
averaged only 17.7 6 6.5 km while random points
averaged 89.5 6 11.5 km (P ¼ 0.03). Taking the entire
potential wintering area into account, penguins averaged
510.4 6 14.6 km south of the ice edge while random
points averaged 619.5 6 16.4 km (P ¼ 0.0001).
Distance to the large-scale ice edge did not vary by
colony (Z ¼ 0.40, P ¼ 0.69), but did vary by year (Z ¼
?3.96, P , 0.0001; Table 1), with 2003 having the
shortest distances and 2005 the longest.
Distance to daylight, amount of light available.—
Winter penguin positions averaged 533.8 6 18.0 km
north of the latitude of zero twilight, 121 km farther
north from this line than randomly generated points (P
, 0.0001; Fig. 4). They averaged 52.6 6 18.0 km south
of the latitude of zero day length, so sunrise/sunset was
not an important determinant of wintering location,
whereas the availability of twilight was. Penguins’
positions averaged 1.27 6 0.10 h of daylight and 5.07
6 0.10 h of twilight, compared with 1.41 6 0.07 and 4.16
6 0.11 h (respectively) for random locations.
The amount of twilight available to wintering
penguins varied by year (Z ¼ ?4.72; P , 0.0001) but
not by colony (Z¼1.32 P¼0.19). Penguins experienced
0.94 and 2.03 fewer twilight hours in 2004 and 2005 than
in 2003, respectively (Table 1).
FIG. 2.
dispersal/pre-molt period, late January to late February, 2004–2006. Penguins from three colonies (Capes Royds, Crozier, and
Beaufort Island, n ¼ 10 individuals total) in the southern Ross Sea were tracked using satellite transmitters (platform transmitter
terminals, PTTs) until batteries failed or PTTs were molted off with feathers. Each color for penguin locations matches the color for
sea ice during February of the same season. The small triangles are simply small amounts of sea ice, coded as for the larger areas. In
general, penguins traveled east-northeast or northeast, usually toward the edge of the pack ice upon leaving the colony. Base map
layers are from British Antarctic Survey (1998). Sea ice data are from the Special Sensor Microwave Imager on board the F13
satellite of the Defense Meteorological Satellite Program, 1 February, 2004–2006.
Ade ´ lie Penguin positions in relation to sea ice distribution (indicated for each year by cross-hatched areas) in the post-
July 20102063PENGUIN MIGRATION AND CLIMATE CHANGE

Page 9

DISCUSSION
Ocean, ice, and biological boundaries
Several factors appear to affect penguin migratory
and winter movements: (1) annual sea ice motion and
extent; (2) the seasonal shortening and lengthening of
daylight; (3) the location of polynyas; (4) the location of
the rich waters of the Antarctic Slope Front (Ainley and
Jacobs 1981, Jacobs 1991); and (5) differences in timing
of departure from the breeding colony. Sea ice dictates
the maximum and mean latitudes where Ross Island
penguins will spend midwinter. As noted by Clarke et al.
(2003) and confirmed by our study, oceanic gyres,
especially during molt when the birds are moving
FIG. 3.
density was calculated from geolocation sensor data for a 100-km grid using the Spatial Analyst extension for ArcGIS version 9.2
(ESRI 2006). Base map layers are from British Antarctic Survey (1998; land and ice shelves), Davey (2004; bathymetry), Orsi et al.
(1995; Antarctic Circumpolar Current [ACC] southern boundary), and U.S. Naval Observatory (hhttp://aa.usno.navy.mil/data/
docs/RS_OneDay.phpi; latitude of zero winter twilight).
Relative wintering density of penguins by colony June–July 2003–2005: (a) Cape Crozier, (b) Cape Royds. Kernel
GRANT BALLARD ET AL.2064Ecology, Vol. 91, No. 7

Page 10

passively on an ice floe, determine much of the migration
route.
Ross Island penguins face the greatest distance of any
Ade ´ lies between their breeding colony and the vicinity of
the Antarctic Circle, the location where sufficient light
and divergent sea ice are reliably available during
midwinter, a distance of 168 latitude (1778 km). In
contrast, Ade ´ lie Penguins studied at Prydz Bay, Princess
Elizabeth Land (698 S; Clarke et al. 2003), Anvers, and
the South Shetland Islands (62–648 S; Fraser and
Trivelpiece 1996), breeding close to if not north of the
Antarctic Circle, would need to travel only as far as the
nearest divergent sea ice. That means for Prydz Bay
birds about 58 latitude north; for Anvers Island birds
about 38 latitude south; and for South Shetland birds,
about 10–158 longitude southeast (equivalent distance to
about 48 latitude). Therefore, as currently there are no
Ade ´ lie Penguin colonies south of 648 S in the Weddell
Sea (Woehler 1993), the Ross Island penguins make the
longest migration of this species, traveling as far as
17600 km round trip between autumn and spring.
Our results are consistent with a previous study
(Emlen and Penney 1964, Penney and Emlen 1967)
showing that displaced penguins from Ross Island
immediately headed NNE, as well as with the study by
Davis et al. (1996, 2001), who tracked post-molt
penguins from Cape Bird, Ross Island (778 S), and
Cape Hallett, Victoria Land (728 S), and showed that in
each instance (n¼3) the birds wintered near the Balleny
Islands. In the latter study, all the birds were among a
very small minority of birds that had molted at the
colonies and thus had a relatively late start on
migration, as was true of the Royds birds in our study.
The difference in timing and direction of departure
between birds in our study (presumably pre-molt) and in
Davis et al. (1996, 2001) (post-molt) is probably due to
difference in ice conditions encountered by the two
groups. The initial NE direction of the pre-molt birds in
our study might also be a way for the birds to
compensate for the northwest circulation of the Ross
Sea Gyre while moving north (Penney and Emlen 1967,
Ainley 2002).
For Ross Island penguins, polynyas may provide
important ‘‘stepping stones’’ on the way to the outer
edge of the pack ice, especially the Pennell and Ross
Passage polynyas (see Jacobs and Comiso 1989), which
are located along the autumn migratory route, and the
Balleny Islands Polynya, one of only a few polynyas in
the Antarctic that is not along the continental coast and
lies closer to the large-scale ice edge. In the autumn and
winter, these stretches of open water are likely to be full
of life (including penguins, seals, whales, and their prey),
although little is known about the mid- to upper-
trophic-level ecology of these open areas in the Antarctic
ice pack (see Smith and Barber 2007).
Timing of departure at Cape Royds is delayed by a
week or more compared to birds at Cape Crozier.
Unique to Cape Royds, at such high latitude, about one-
third or more of the population also molt at the colony
(Taylor 1962). This means that departure may be
delayed by as much as a month compared to Cape
Crozier. Birds that depart later are likely to encounter
more consolidated pack ice, but also a stream of
relatively rapidly northward-moving ice in the western
Ross Sea (Appendix C; also see Jeffries and Kozlenko
[2002], who report monthly average buoy drift up to 16
km/d in this area). In any case, the fact that they usually
spend the winter 88 west of Crozier penguins means that
their return to Cape Royds may more commonly be
against a stronger flow of ice than what Crozier
penguins encounter (Appendix C). It also might mean
that they spend their winters in the vicinity of many
more penguins from other colonies, with potential
consequences to food availability (Ainley et al. 2004)
and energy expenditure (Ballance et al. 2009). However,
return trip travel speeds for Royds penguins did not
differ from Crozier penguins, so if they were handi-
capped by fighting stronger currents, they were able to
compensate, potentially by expending more energy. This
could help to explain why Cape Royds phenology is
FIG. 4.
(June–July 2003–2005). (A) Kernel density in relation to ice
concentration for 253 penguin locations compared with 630
random locations. Kernel densities of real and randomly
generated positions were estimated for the full range of sea
ice concentration possible (for each 2% increment, 0–100%)
using the Epanechnikov kernel function to extrapolate distri-
butions from the samples. (B) Penguin locations in relation to
distance from the latitude of zero twilight.
Characteristics of penguin wintering locations
July 2010 2065PENGUIN MIGRATION AND CLIMATE CHANGE

Page 11

delayed compared to Cape Crozier, and may also have
negative consequences to over-winter survival (K.
Dugger, D. Ainley, and G. Ballard, unpublished data).
It does not seem to affect breeding success or fledging
mass of chicks (Ainley et al. 2004). We did not discover
any other differences in wintering area characteristics
between the two colonies at the scale permitted by our
methods.
Wintering areas of Ross Island penguins were at the
edge of the consolidated pack ice (and the edge of
darkness), well back from the large-scale ice edge itself.
This was contrary to our expectations, which were based
on a previous winter observation that Ade ´ lie Penguins
were most concentrated in a belt ;100 km inside the
large-scale edge, but not necessarily at the edge of the
consolidated pack in the Weddell Sea; they appeared to
be avoiding only the outermost area where ice extent
expands and contracts weekly, depending on wind
strength and direction (Ainley et al. 1993). Judging
from the eastward gradient in longitudinal dispersion of
penguins, these birds originated from colonies at the tip
of the Antarctic Peninsula (Ainley et al. 1993).
Assuming that Ross Sea penguins could also occupy a
habitat of relatively lower ice concentration, there
potentially exists a wide swath with few Ross Island
penguins between the 75–85% ice cover where we found
them wintering and the 15% ice edge farther north. One
factor that could help to explain this pattern, and the
differences from that of the Weddell Sea, is the probable
unusually high density of penguins in this more northern
extent of the Ross Sea pack. Of the world’s population
of Ade ´ lie Penguins, 30% (i.e., 1.5 million breeders, plus
nonbreeders) are associated with the northern Victoria
Land colonies (e.g., Cape Hallett north to Cape Adare)
compared to fewer penguins found over a much larger
area in the western Weddell Sea (1.1 million breeders)
from the South Shetlands, South Orkneys, and northern
Antarctic Peninsula coast (see Woelher 1993). In other
words, we hypothesize that the Ross Island/southern
Victoria Land penguins (0.75 million breeders) would
winter farther north were it not for the probable
presence of huge numbers of penguins from northern
Victoria Land already wintering there, because we have
shown that penguins adjust their foraging areas in
response to both inter- and intraspecific competition
(Ainley et al. 2004, 2006). However, it is also possible
that the Ross Island penguins simply try to stay as close
to their home colonies as possible, given light and ice
conditions, reducing the amount of time and energy
required to return for breeding. In addition, they appear
to remain, as long as ice conditions allow, in the vicinity
of the Ross Sea continental slope and the Antarctic
Slope Front, an exceedingly rich area (Ainley et al.
1984). No studies on the migration of Ade ´ lie Penguins in
northern Victoria Land have been conducted to address
these hypotheses.
In years of more extensive ice, the zone of consoli-
dated ice shifts north (sea ice extent and sea ice
concentration covary at the large scale; Jacobs and
Comiso 1989, Stammerjohn et al. 2008) and, as we
observed, shifts the wintering area of Ross Island
penguins farther north as well. This would move the
penguins away from the Slope Front and closer to the
ACC Southern Boundary, across which there is less food
available (Tynan 1998, Nicol et al. 2000), and perhaps
would also add to the density of the northern Victoria
Land wintering penguins.
Astronomical boundaries
Our finding that the penguins are limited by the
availability of twilight, and not necessarily daylight, is
consistent with the findings of Emlen and Penney (1964)
and Penney and Emlen (1967), who found that Ade ´ lie
Penguins’ navigational ability is challenged by the lack
of sunlight. As they and others have noted (summarized
in Ainley 2002), penguins remain in place where they
have no geographic navigational cues and when the sun
is not shining. The slow northward migration of Ross
Island penguins in our study is probably the result of
being advected with the ice upon which they spend most
of a day, rather than swimming and actually navigating.
The fact that the penguins travel much more quickly
when going south during the spring migration, much
faster than ice motion, is consistent with movement
guided by sun navigation.
However, Ade ´ lies (and all penguins) require some
light in order to forage, although apparently less than is
required for navigation. Wilson et al. (1993) found that
Ade ´ lies made most of their foraging dives to depths
where there was at least 1 lux of light available, and that
foraging depth and success were much lower during
darkness than during daylight. The range of light
available at the surface during civil twilight ranges from
3.4 to 400 lux (Bond and Henderson 1963), so some
shallow diving would be possible even at the darkest end
of this range; during darker hours, prey are likely to
migrate closer to the surface, where they would be
silhouetted against the surface/sky (Wilson et al. 1993,
Fuiman et al. 2002).
Migration and long-term sea ice variability
The ability to migrate over the long distances
exhibited by Ross Island Ade ´ lie Penguins may be an
ongoing adaptation in the evolution of the species, and
(if such adaptation has a genetic basis, as has been
shown in at least one other organism; Zhu et al. 2009)
seemingly within the genetic plasticity documented at
the millennial (1000-yr) timescale for this species
(Shepherd et al. 2005). At the Last Glacial Maximum
(LGM, ;19000 yr BP), the West Antarctic Ice Sheet
(WAIS) covered most of the Ross Sea (Anderson 1999).
Given that the Ross Sea Ade ´ lie Penguin has a genome
that differs from members of this species in all other
regions (Roeder et al. 2001), and that any offshore
islands in the Pacific sector (of which there are very few)
were almost certainly ice covered (e.g., Balleny Islands,
GRANT BALLARD ET AL.2066 Ecology, Vol. 91, No. 7

Page 12

Scott Island; Anderson 1999), a Ross Sea colony
probably existed during the LGM. Ainley (2002)
proposed that Cape Adare was the likely location,
because the northwest corner of the Ross Sea has been
ice-sheet-free during recent glaciations, unlike the
continental shelf everywhere else (which had grounded
ice sheets to the shelf break; Anderson 1999), and
sediment cores from the vicinity indicate a polynya there
(Thatje et al. 2008). Moreover, Cape Adare has been
free of land ice for ;16000 yr (Johnson et al. 2008), i.e.,
going back to nearly the ice maximum and before retreat
of the WAIS across the Ross Sea began. Although
evidence of colonies near Cape Adare from this time
period has not been discovered, such locations may now
be underwater as a result of the 120-m sea level rise since
the LGM (an option in data interpretation left open by
Emslie et al. [2007]). Beginning about 12000 yr BP, the
WAIS began to withdraw south, exposing new, suitable
nesting habitat along the Victoria Land coast. Ade ´ lie
Penguins colonized the Victoria Land coastline sporad-
ically southward, depending on sea ice concentration
(Emslie et al. 2003, 2007), breeding farther and farther
from the large-scale winter sea ice edge, the Antarctic
Circle, and winter daylight. However, at the southern-
most extent of the current range (Cape Royds), the
penguin breeding period is already significantly shorter
than at colonies farther north, and probably could not
be shortened further (Ainley 2002). Therefore it seems
unlikely that this species would colonize terrain south of
the current WAIS boundary, were it available, even if
the species is forced to retreat from lower latitudes as sea
ice disappears (Ainley et al. 2010).
In summary, the life history patterns of the Ade ´ lie
Penguin have been in a state of flux, owing largely to
adjustments in migratory behavior and routes. Although
the species apparently has contended with this success-
fully throughout its 3 million year history, as ice ages
have come and gone with coincident changes in breeding
and sea ice habitat, the current rate of habitat change
may be unprecedented for this species. We predict that
the response of Ade ´ lie Penguins to the large-scale
decrease in sea ice projected by climate models (Ainley
et al. 2010) will be affected by migratory adjustments to
the spatial availability of light before the pack ice
disappears entirely.
ACKNOWLEDGMENTS
The work of G. Ballard, V. Toniolo, and D. Ainley was
funded by NSF grant OPP 0440643, with very proficient logistic
support provided by the U.S. Antarctic Program. G. Ballard
received additional support from the University of Auckland,
School of Biological Sciences. The participation of K. Arrigo
was supported by NASA grant NNG05GR19G. For assistance
with fieldwork since 2003, we thank Louise Blight, Jennifer
Blum, Katie Dugger, Carina Gjerdrum, Michelle Hester,
Ame ´ lie Lescroe ¨ l, Chris McCreedy, Rachael Orben, Vijay Patil,
Ben Saenz, and Lisa Sheffield. Shulamit Gordon kindly placed
reference tags at Cape Hallett, and Gert van Dijken and Nick
DiGirolamo helped with ice data processing. Mark Hauber and
Katie Dugger provided reviews of earlier drafts. The paper
benefitted greatly from peer review by C. A. Bost and an
anonymous reviewer. This is PRBO contribution #1696.
LITERATURE CITED
Afanasyev, V. 2004. A miniature daylight level and activity data
recorder for tracking animals over long periods. Memoirs of
National Institute of Polar Research 58:227–233.
Ainley, D. G. 2002. The Ade ´ lie Penguin: bellwether of climate
change. Columbia University Press, New York, New York,
USA.
Ainley, D. G., G. Ballard, and K. M. Dugger. 2006.
Competition among penguins and cetaceans reveals trophic
cascades in the western Ross Sea, Antarctica. Ecology 87:
2080–2093.
Ainley, D. G., F. O. C. Edmund, and R. J. Boekelheide. 1984.
The marine ecology of birds in the Ross Sea, Antarctica.
American Ornithologists’ Union. Ornithological Mono-
graphs 32.
Ainley, D. G., and W. B. Emison. 1972. Sexual size dimorphism
in Ade ´ lie penguins. Ibis 114:267–271.
Ainley, D. G., and S. S. Jacobs. 1981. Affinity of seabirds for
ocean and ice boundaries in the Antarctic. Deep-Sea
Research 28A:1173–1185.
Ainley, D. G., R. E. LeResche, and W. J. L. Sladen. 1983.
Breeding biology of the Ade ´ lie penguin. University of
California Press, Berkeley, California, USA.
Ainley, D. G., C. A. Ribic, G. Ballard, S. Heath, I. Gaffney, B.
Karl, K. J. Barton, P. R. Wilson, and S. Webb. 2004.
Geographic structure of Ade ´ lie Penguin populations: overlap
in colony-specific foraging areas. Ecological Monographs 74:
159–178.
Ainley, D. G., C. A. Ribic, and W. R. Fraser. 1994. Ecological
structure among migrant and resident seabirds of the Scotia–
Weddell confluence region. Journal of Animal Ecology 63:
347–364.
Ainley, D. G., C. A. Ribic, and L. B. Spear. 1993. Species–
habitat relationships among Antarctic seabirds: a function of
physical or biological factors? Condor 95:806–816.
Ainley, D. G., J. Russell, S. Jenouvrier, E. Woehler, P. O. B.
Lyver, W. R. Fraser, and G. L. Kooyman. 2010. Antarctic
penguin response to habitat change as Earth’s troposphere
nears 28C above preindustrial levels. Ecological Monographs
80:49–66.
Alerstam, T., A. Hedenstroem, and S. Akesson. 2003. Long-
distance migration: evolution and determinants. Oikos 103:
247–260.
Anderson, J. B. 1999. Antarctic marine geology. Cambridge
University Press, Cambridge, UK.
Arrigo, K. R., G. L. van Dijken, and S. Bushinsky. 2008.
Primary production in the Southern Ocean, 1997–2006.
Journal of Geophysical Research 113:C08004. [doi: 10.
1029/2007JC004551]
Arrigo, K. R., D. Worthen, A. Schnell, and M. P. Lizotte. 1998.
Primary production in Southern Ocean waters. Journal of
Geophysical Research 103:15587–15600.
Ballance, L. T., D. G. Ainley, G. Ballard, and K. Barton. 2009.
An energetic correlate between colony size and foraging
effort in seabirds, an example of the Ade ´ lie penguin
Pygoscelis adeliae. Journal of Avian Biology 40:279–288.
Ballard, G., D. Ainley, C. Ribic, and K. Barton. 2001. Effect of
instrument attachment and other factors on foraging trip
duration and nesting success of Ade ´ lie Penguins. Condor 103:
481–490.
Barbraud, C., and H. Weimerskirch. 2003. Climate and density
shape population dynamics of a marine top predator.
Proceedings of the Royal Society B 270:2111–2116.
Bond, D. S., and F. P. Henderson. 1963. The conquest of
darkness. (AD 346297). Defense Documentation Center,
Alexandria, Virginia, USA.
July 2010 2067 PENGUIN MIGRATION AND CLIMATE CHANGE

Page 13

British Antarctic Survey. 1998. Antarctic digital database.
Version 2.0. Manual and bibliography. Scientific Committee
on Antarctic Research, Cambridge, UK.
Brown, C. R. 1987. Traveling speed and foraging range of
Macaroni and Rockhopper Penguins at Marion Island.
Journal of Field Ornithology 58:118–125.
Cavalieri, D., C. Parkinson, P. Gloersen, and H. J. Zwally.
2006. Sea ice concentrations from Nimbus-7 SMMR and
DMSP SSM/I passive microwave data, Dec. 17 1997 to Jan.
22 2007. National Snow and Ice Data Center, Boulder,
Colorado USA. hhttp://nsidc.org/data/nsidc-0051.htmli
Clapham, P. J., and D. K. Mattila. 1990. Humpback whale
songs as indicators of migration routes. Marine Mammal
Science 6:155–160.
Clark, B. D., and W. Bemis. 1979. Kinematics of swimming of
penguins at the Detroit Zoo. Journal of Zoology 188:411–
428.
Clarke, J. R., K. Kerry, C. Fowler, R. Lawless, S. Eberhard,
and R. Murphy. 2003. Post-fledging and winter migration of
Ade ´ lie penguins Pygoscelis adeliae in the Mawson region of
East Antarctica. Marine Ecology Progress Series 248:267–
278.
Cline, D. R., D. B. Siniff, and A. W. Erickson. 1969. Summer
birds of the pack ice in the Weddell Sea, Antarctica. Auk 86:
701–716.
Cockell, C. S., M. D. Stokes, and K. E. Korsmeyer. 2000.
Overwintering strategies of Antarctic organisms. Environ-
mental Review 8:1–19.
Cox, N. J. 1998. CIRCSTAT: Stata modules to calculate
circular statistics. Statistical Software Components S362501.
Boston College Department of Economics, Boston, Massa-
chusetts, USA. hhttp://ideas.repec.org/c/boc/bocode/s362501.
htmli
Davey, F. J. 2004. Ross Sea bathymetry, 1:2,000,000. Version
1.0. Geophysical map 16. Institute of Geological and Nuclear
Sciences, Lower Hutt, North Island, New Zealand.
Davis, L. S., P. D. Boersma, and G. S. Court. 1996. Satellite
telemetry of the winter migration of Ade ´ lie penguins
(Pygoscelis adeliae). Polar Biology 16:221–225.
Davis, L. S., R. G. Harcourt, and C. J. Bradshaw. 2001. The
winter migration of Ade ´ lie penguins breeding in the Ross Sea
sector of Antarctica. Polar Biology 24:593–597.
Dugger, K. M., G. Ballard, D. G. Ainley, and K. J. Barton.
2006. Effects of flipper bands on foraging behavior and
survival of Ade ´ lie Penguins (Pygoscelis adeliae). Auk 123:
858–869.
Emlen, J. T., and R. L. Penney. 1964. Distance navigation in
the Ade ´ lie penguin. Ibis 106:417–431.
Emslie, S. D., P. A. Berkman, D. G. Ainley, L. Coats, and M.
Polito. 2003. Late-Holocene initiation of ice-free ecosystems
in the southern Ross Sea, Antarctica. Marine Ecology
Progress Series 262:19–25.
Emslie, S. D., L. Coats, and K. Licht. 2007. A 45,000 yr record
of Ade ´ lie penguins and climate change in the Ross Sea,
Antarctica. Geology 35:61–64.
Emslie, S. D., W. Fraser, R. C. Smith, and W. Walker. 1998.
Abandoned penguin colonies and environmental change in
the Palmer station area. Anvers Island, Antarctic Peninsula.
Antarctic Science 10:257–268.
ESRI. 2006. ArcGIS. Version 9.2. Environmental Systems
Research Institute, Redlands, California, USA.
Fraser, W. R., and W. Z. Trivelpiece. 1996. Factors controlling
the distribution of seabirds: winter–summer heterogeneity in
the distribution of Ade ´ lie penguin populations. Pages 257–
272 in R. Ross, E. Hofmann, and L. Quetin, editors.
Foundations for ecological research west of the Antarctic
Peninsula. Antarctic Research Series 70. American Geophys-
ical Union, Washington, D.C., USA.
Fuiman, L., R. Davis, and T. Williams. 2002. Behavior of
midwater fishes under the Antarctic ice: observations by a
predator. Marine Biology 140:815–822.
Greenberg, R., and P. P. Marra. 2005. Birds of two worlds: the
ecology and evolution of migration. Johns Hopkins Univer-
sity Press, Baltimore, Maryland, USA.
Hill, R. D. 1994. Theory of geolocation by light levels. Pages
227–236 in B. J. Le Boeuf and R. M. Laws, editors. Elephant
seals: population ecology, behavior, and physiology. Univer-
sity of California Press, Berkeley, California, USA.
Jacobs, S. S. 1991. On the nature and significance of the
Antarctic Slope Front. Marine Chemistry 35:9–24.
Jacobs, S. S., and J. C. Comiso. 1989. Sea ice and oceanic
process on the Ross Sea continental shelf. Journal of
Geophysical Research 94:18195–18211.
Jacobs, S. S., C. F. Giulivi, and P. A. Mele. 2002. Freshening of
the Ross Sea during the late 20th century. Science 297:386–
389.
Jeffries, M. O., and N. Kozlenko. 2002. Buoy deployments in
the Ross Sea pack ice, 1998 and 1999. Appendix D (vi) in
Report on the Third Meeting of Programme Participants,
International Programme for Antarctic Buoys (IPAB).
World Climate Research Programme, Informal Report
Number 5/2002, Geneva, Switzerland.
Johnson, J. S., C. D. Hillenbrand, J. L. Smellie, and S. Rocchi.
2008. The last deglaciation of Cape Adare, northern Victoria
Land, Antarctica. Antarctic Science 20:581–587.
Kerry, K., D. Agnew, J. Clarke, and G. Else. 1992. Use of
morphometric parameters for the determination of sex of
Ade ´ lie penguins. Wildlife Research 19:657–664.
McConnell, B. J., and M. A. Fedak. 1996. Movements of
southern elephant seals. Canadian Journal of Zoology 74:
1485–1496.
Nicol, S., T. Pauly, N. L. Bindoff, S. Wright, D. Thiele, G. W.
Hosie, P. G. Strutton, and E. Woehler. 2000. Ocean
circulation off east Antarctica affects ecosystem structure
and sea-ice extent. Nature 406:504–507.
Orsi, A. H., T. Whitworth, and W. D. Nowlin. 1995. On the
meridional extent and fronts of the Antarctic Circumpolar
Current. Deep Sea Research Part I: Oceanographic Research
Papers 42:641–673.
Parkinson, C. L. 2002. Trends in the length of the Southern
Ocean sea-ice season, 1979–99. Annals of Glaciology 34:435–
440.
Parmelee, D. F., W. R. Fraser, and D. R. Neilson. 1977. Birds
of the Palmer Station area. Antarctic Journal of the United
States 12:15–21.
Penney, R. L., and J. T. Emlen. 1967. Further experiments on
distance navigation in the Ade ´ lie penguin Pygoscelis adeliae.
Ibis 109:99–109.
Phillips, R. A., J. R. D. Silk, J. P. Croxall, V. Afanasyev, and
V. J. Bennett. 2005. Summer distribution and migration of
nonbreeding albatrosses: individual consistencies and impli-
cations for conservation. Ecology 86:2386–2396.
Phillips, R. A., J. R. D. Silk, J. P. Croxall, V. Afanasyev, and
D. R. Briggs. 2004. Accuracy of geolocation estimates for
flying seabirds. Marine Ecology Progress Series 266:265–272.
Roeder, A., R. K. Marshall, A. J. Mitchelson, T. Visagathila-
gar, P. A. Ritchie, D. R. Love, T. J. Pakai, H. C. McPartlan,
N. D. Murray, N. A. Robinson, K. R. Kerry, and D. M.
Lambert. 2001. Gene flow on the ice: genetic differentiation
among Ade ´ lie penguin colonies around Antarctica. Molecu-
lar Ecology 10:1645–1656.
Shepherd, L. D., C. D. Millar, G. Ballard, D. G. Ainley, P. R.
Wilson, G. D. Haynes, C. Baroni, and D. M. Lambert. 2005.
Microevolution and mega-icebergs in the Antarctic. Proceed-
ings of the National Academy of Sciences USA 102(46):
16717–16722.
Smith, W. O., and D. G. Barber, editors. 2007. Polynyas:
windows to the world. Elsevier Publishers, London, UK.
Stammerjohn, S., D. Martinson, R. Smith, X. Yuan, and
D. H. Rind. 2008. Trends in Antarctic annual sea ice retreat
and advance and their relation to El Ni˜ no–Southern
GRANT BALLARD ET AL.2068Ecology, Vol. 91, No. 7

Page 14

Oscillation and Southern Annular Mode variability. Journal
of Geophysical Research 113:C03S90.
Stata Corporation. 2008. STATA statistical software. Release
10.1. Stata Corporation, College Station, Texas, USA.
Taylor, R. H. 1962. The Ade ´ lie penguin Pygoscelis adeliae at
Cape Royds. Ibis 104:76–204.
Thatje, S., C. D. Hillenbrand, A. Mackensen, and R. Larter.
2008. Life hung by a thread: endurance of Antarctic fauna in
glacial periods. Ecology 89:682–692.
Trathan, P. N., J. P. Croxall, and E. J. Murphy. 1996.
Dynamics of Antarctic penguin populations in relation to
inter-annual variability in sea ice distribution. Polar Biology
16:321–330.
Turner, J., J. C. Comiso, G. J. Marshall, T. A. Lachlan-Cope,
T. Bracegirdle, T. Maksym, M. P. Meredith, Z. Wang, and
A. Orr. 2009. Non-annular atmospheric circulation change
induced by stratospheric ozone depletion and its role in the
recent increase of Antarctic sea ice extent. Geophysical
Research Letters 36:L08502.
Tynan, C. T. 1998. Ecological importance of the southern
boundary of the Antarctic Circumpolar Current. Nature 392:
708.
Wilson, P. R., D. G. Ainley, N. Nur, S. S. Jacobs, K. J. Barton,
G. Ballard, and J. C. Comiso. 2001. Ade ´ lie penguin
population change in the Pacific Sector of Antarctica:
relation to sea-ice extent and the Antarctic Circumpolar
Current. Marine Ecology Progress Series 213:301–309.
Wilson, R. P., K. Pu ¨ tz, C. A. Bost, B. M. Culik, R. Bannasch,
T. Reins, and D. Adelung. 1993. Diel dive depth in penguins
in relation to diel vertical migration of prey: whose dinner by
candlelight? Marine Ecology Progress Series 94:101–104.
Wilson, R. P., and M. P. Wilson. 1989. Tape: a package
attachment technique for penguins. Wildlife Society Bulletin
17:77–79.
Woehler, E. J. 1993. The distribution and abundance of
antarctic and subantarctic penguins. Scientific Committee
for Antarctic Research, Scott Polar Research Institute,
Cambridge, UK.
Zhu, H., R. J. Gegear, A. Casselman, S. Kanginakudru, and
S. M. Reppert. 2009. Defining behavioral and molecular
differences between summer and migratory monarch butter-
flies. BMC [BioMedCentral] Biology 7:14.
Zwally, H. J., J. C. Comiso, C. L. Parkinson, D. J. Cavalieri,
and P. Gloersen. 2002. Variability of Antarctic sea ice 1979–
1998. Journal of Geophysical Research 107(C5):3041.
APPENDIX A
A table showing GLS (geolocation sensor) deployment and retrieval dates, locations, and sample sizes (Ecological Archives
E091-142-A1).
APPENDIX B
A figure showing GLS-derived penguin locations and sea ice concentration and extent, 2003–2005 (Ecological Archives E091-
142-A2).
APPENDIX C
A figure showing monthly average ice flow vectors for March, June, and September 2003 (Ecological Archives E091-142-A3).
July 20102069PENGUIN MIGRATION AND CLIMATE CHANGE

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Ecological Archives E091-142-A1
Grant Ballard, Viola Toniolo, David G. Ainley, Claire L. Parkinson, Kevin R.
Arrigo, Phil N. Trathan. YEAR. Responding to climate change: Adélie Penguins
confront astronomical and ocean boundaries. Ecology 91: 2056-2069.
Appendix A (table A1). GLS (geolocation sensor) deployment and recovery locations, timing, and sex for Adélie
penguins on Ross Island. Number retrieved functioning is listed in parentheses, 3 more tags were retrieved after 2
-3 winters but were not included in these analyses.
DateLocation# Deployed# Retrieved after 1 winter
Male Female Unk.Male FemaleUnk.
Jan. 2003C. Crozier 135012 (7)4 (1)0
Feb. 2003C. Royds6405 (1)2 (2)0
Jan. 2004C. Crozier7943 (2) 6 (3)4 (3)
Jan. 2004C. Royds71405 (2) 7 (3)0
Jan. 2004 C. Crozier Reference tags (3)
Jan. 2004C. Hallett Reference tags (3)
Jan. 2005 C. Crozier11637 (5) 4 (3)2 (2)
Jan. 2005 C. Royds7354 (4)2 (2)1 (1)
Totals 514112 37 (16) 25 (13)7 (4)
104 total deployed 68 total retrieved (41 functioning)

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