A comprehensive coastal seabird survey maps out the front ...€¦ · A comprehensive coastal seabird survey maps out the front lines ... response to changing sea ice and prey distributions,

ORIGINAL PAPER

A comprehensive coastal seabird survey maps out the front linesof ecological change on the western Antarctic Peninsula

Paula Casanovas · Ron Naveen · Steve Forrest ·Jérôme Poncet · Heather J. Lynch

Received: 16 October 2014 / Revised: 14 January 2015 / Accepted: 25 January 2015

© Springer-Verlag Berlin Heidelberg 2015

Abstract Seabirds along the western Antarctic Peninsula

are known to be shifting in abundance and distribution in

response to changing sea ice and prey distributions, but the

spatial extent of these changes has remained an open

question because survey efforts have focused on the more

easily accessed northern coastline. We used a yacht-based

field expedition (January 5–21, 2013) to complete the first

comprehensive penguin (Pygoscelis spp.) and blue-eyed

shag (Phalacrocorax [atriceps] bransfieldensis) populationsurvey of the Graham and Loubet Coasts of the western

Antarctic Peninsula since the mid-1980s. Our surveys

document a sharp transition zone at the northern boundary

of Marguerite Bay; north of this boundary zone, we con-

firm widespread declines in Adelie penguins and increasing

populations of gentoo penguins, but south of this zone we

find Adelie populations that have remained stable or

increased in abundance since the previous surveys by

Poncet and Poncet (Br Antarct Surv Bull 77:109–129,

1987). Marguerite Bay has long been known as a predator

“hotspot,” but our findings suggest that Marguerite Bay has

actually been improving for marine predators for at least

several decades. Marguerite Bay, which has fundamentally

different ocean dynamics than in areas just outside Mar-

guerite Bay, has maintained persistent phytoplankton

blooms over the past decade even as summer sea ice extent,

which can inhibit access to breeding areas, has declined.

This provides further support for the hypothesis that ocean

productivity and sea ice dynamics are critical factors reg-

ulating Adelie penguin abundance in the region and that

Marguerite Bay is now at the front lines of ecological

change in this region.

Keywords Penguins · Blue-eyed shag · Marguerite

Bay · Sea ice · Phytoplankton blooms

Introduction

It is now well established that penguin populations on the

Antarctic Peninsula have been changing over the past three

decades (Trivelpiece et al. 2011; Lynch et al. 2012;

Ducklow et al. 2013). Particular attention has focused on

widespread declines in the abundance of Adelie penguin

(Pygoscelis adeliae) colonies situated along the western

coast of the Antarctic Peninsula (Lynch et al. 2012; Lynch

and LaRue 2014), as well as increasing abundance and

southward expansion of gentoo penguins (P. papua) (Lynchet al. 2012). Evidence suggests that environmental factors

associated with climate change, such as declining sea ice

and shifts in primary productivity, play a significant role in

these shifting patterns of abundance and distribution (Fra-

ser et al. 1992; Smith et al. 1999; Croxall et al. 2002;

Clarke et al. 2007; Murphy et al. 2007; Trivelpiece et al.

2011). Most studies to date, however, have focused on

colonies north of 65°S, and thus information on population

changes south of 65°S and in the vicinity of Marguerite

Bay has been limited. The survey work reported by Poncet

Electronic supplementary material The online version of thisarticle (doi:10.1007/s00300-015-1651-x) contains supplementarymaterial, which is available to authorized users.

P. Casanovas · R. Naveen · S. Forrest

Oceanites, Inc., Chevy Chase, MD, USA

J. Poncet

Golden Fleece Expedition Cruises, Beaver Island,

Falkland Islands

H. J. Lynch (&)

Ecology and Evolution Department, Stony Brook University,

Stony Brook, NY 11794, USA

e-mail: [email protected]

123

Polar Biol

DOI 10.1007/s00300-015-1651-x

and Poncet (1987), who censused penguin colonies in this

region from 1983 to 1987, is the only comprehensive field

survey of the region prior to that reported here. Their data

provide the baseline against which we can assess changes

in the abundance and distribution of penguins breeding

south of 65°S on the western Antarctic Peninsula (WAP).

Monitoring seabird populations in the Antarctic is

important because changes in their abundance and distri-

bution may indicate regional climate change (Croxall et al.

2002) or direct or indirect human disturbance (e.g., tour-

ism, marine traffic, commercial harvesting of marine

resources). However, limited data south of 65°S have made

it impossible to know whether observed changes persist

south of the latitudinal range for which data have been

available. Lynch et al. (2012) found that while Adelie

penguins were declining over most of the western Antarctic

Peninsula (WAP), populations at Bongrain Point, Pourquoi

Pas Island (−67.72°, −67.73°) and Red Rock Ridge

(–68.29°, −67.18°) were actually increasing. At the same

time, gentoo penguins were found to be expanding their

range further south, prompting Lynch et al. (2012) to

predict further expansion south to the Berthelot Islands.

More recent evidence suggests that chinstrap penguins (P.antarctica), which are declining regionally (e.g., Lynch

et al. 2012), may also be establishing new colonies at their

southern range margin (~65°S), although only in areas

already occupied by other pygoscelid penguins (Lynch

et al. 2013). To address these open questions, we organized

a multipronged survey of the Graham and Loubet Coasts

(between 65° and 68° South, including the Marguerite Bay

area) using a comprehensive yacht-based field survey of

the region supported by a coastal survey of high-resolution

satellite imagery. While most of the WAP is being moni-

tored regularly (Lynch et al. 2013), the area south of 65°Sis not routinely visited by passenger vessels. Small yacht

operations allow for the surveying of areas that are extre-

mely difficult or impossible to reach by bigger vessels and

provide greater flexibility for scheduling travel among

sites.

Methods

Field survey

From January 5 to 21, 2013, we used the yacht GoldenFleece (with a 19.5 m steel hull, a beam of 6.19 m, and a

maximum draft of 2.48 m) to survey the WAP coastline

between 65°06′ and 68°18′S, including offshore islands in

the Grandidier Channel, Crystal Sound, the west and

southern coast of Adelaide Island, and the islands in

Marguerite Bay (Fig. 1). Over this period, we completed 43

site censuses, where some sites included multiple census

locations due to dispersal of individuals over small island

archipelagos or islands separated from the mainland. Ide-

ally, each “site” encompasses a single breeding population,

but we have defined their boundaries and naming schema

to remain consistent with historical precedent. Mild

weather conditions and the absence of pack ice facilitated

the work, allowing for surveying every day and access to

all targeted sites. We surveyed all of the known breeding

locations described in Poncet and Poncet (1987) south of

Moot Point except for Rhyolite Island (69°40′S, 68°47′W),

which could not be reached because of time/ice constraints

and distance. The survey occurred after the peak of pen-

guin egg-laying (for nest counts) and before the peak of

penguin chick-creching (for chick counts). We mapped,

through waypoints and tracklogs as appropriate, all sur-

veyed sites, as well as the Golden Fleece’s route.We systematically searched all known or discovered

islands, islets, and penguin/shag colonies thereon, relying

upon Capt. Jerome Poncet’s [30 years experience navi-

gating these waters and on his navigation notes from the

surveys described in Poncet and Poncet (1987). With the

exception of the shag survey at Green Island, all of our

surveys were accomplished by researchers (PC, RN, and

SF) on land, proceeding from Golden Fleece to shore by

zodiac. All encountered colonies of gentoo penguins,

chinstrap penguins, Adelie penguins, and blue-eyed shags

were mapped and censused by direct enumeration of

individual occupied nests or chicks [see Lynch et al. (2008)

for details on survey methodology]. We counted nests or

chicks individually three times and report the average of

those three counts; estimates of abundance are, except as

noted, accurate to ±5 %. We focused our survey on pen-

guin breeding sites reported by Poncet and Poncet (1987)

and the Wildlife Awareness Manual (Harris 2006), as well

as at locations that had been determined by remotely

sensed data to potentially contain rookeries.

Gentoo penguins were counted at eight census sites. All

gentoo penguins were past the peak of egg-laying, many

brooding 1–2 week old chicks, and no creching was

observed. In this circumstance, the focus throughout was

on obtaining nest counts. Chinstrap penguins were cens-

used at seven locations and found breeding in small

numbers. Only nests with eggs or 1–2 week old chicks

were observed, and thus, the focus was nest counts. Adelie

penguins were censused at 31 census sites. Adelies were

past the peak of egg-laying, with many chicks already

hatched (mostly 2–4 weeks of age) but not yet starting to

creche, so we focused on nest counts. However, at five sites

in Marguerite Bay (Red Rock Ridge, Lagotellerie Island,

Avian Island, Chatos Island, and Cone Island), a significant

proportion of the colony had creched and we counted

chicks instead of occupied nests. Where it was possible to

do so, both occupied nests and chicks were simultaneously

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8 km0 4

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Fig. 1 Track of the GoldenFleece route representing the

area searched and surveyed for

this study. Areas along this track

not reported in this paper

represent true absence within

the detection limits of the

survey (up to 5 km). a Gerlache

Strait area, b Lemaire Channel

to Green Island area, c Renaud

Island area, d Crystal Sound

area, e Marguerite Bay area.

The numbers on the maps

correspond to the Map ID

numbers in Table 1. All imagery

Copyright (2014) by Digital

Globe, Inc.

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123

censused. We also surveyed all blue-eyed shag (Phala-crocorax [atriceps] bransfieldensis) nests in the region.

Data collected by Poncet and Poncet (1987) were similar

in methodology, though the earlier survey included some

estimates obtained from offshore aboard a yacht as

reflected in their lower precision. Our assessment of pop-

ulation change is based on all the available data for each

site surveyed, including data from Poncet and Poncet

(1987), the Antarctic Site Inventory database (Naveen and

Lynch 2011), and other published sources.

Environmental drivers of Adelie population change

We analyzed changes in penguin abundance in the context of

the oceanographic characteristics of the study area, in par-

ticular the patterns of phytoplankton blooms and summer sea

ice extent. Phytoplankton blooms were quantified using the

merged satellite measurements of ocean chlorophyll-a data

derived from the moderate resolution imaging spectroradi-

ometer (MODIS), in orbit on theAqua platform, and the Sea-

viewing Wide Field-of-View Sensor (SeaWIFS), in orbit on

the OrbView-2. We used the level 3 monthly merged chlo-

rophyll product (concentration of chlorophyll-a in mg/m3),

with a spatial resolution of 9 km2. The data were obtained

from the Ocean Biology Processing Group (OBPG), Global

Change Data Center, Earth Sciences Division, Science and

Exploration Directorate, Goddard Space Flight Center,

NASA (http://oceancolor.gsfc.nasa.gov) in hierarchical data

format and converted to ASCII format using ESRI Arc-

GIS10.0. We traced a circular buffer around each colony,

with radius (50 km) equal to the maximum Adelie foraging

distance (Trivelpiece et al. 1987). We calculated the mean

values for chlorophyll-a concentration over a period of

10 years for the month of January, in the over-water portion

of the buffer. Due to small sample size and non-normality

in the within-group distribution of chlorophyll-a concen-

tration, differences between Adelie penguin colonies

increasing in abundance and decreasing in abundance were

assessed using a permutation test (n = 999 random permu-

tations of the values between the “increasing” and

“decreasing” categories).

Sea ice spatiotemporal distribution was estimated from

NIMBUS-7 Scanning Multichannel Microwave Radiome-

ter (SMMR) and the Defense Meteorological Satellite

Programs (DMSP) Special Sensor Microwave/Imager

(SSM/I) and the Special Sensor Microwave Imager/Soun-

der (SSMIS) passive microwave data (25 km2 spatial

resolution). The data were obtained from the National

Snow and Ice Data Center in raw binary format and con-

verted to ASCII format using ESRI ArcGIS 10.0. We

calculated the minimum sea ice concentration for the

month of December for the same buffers described above

from 1978 to 2011.

Results

Field survey

The list of sites visited along with the presence–absence

summary for each site (describing the status of the colony

if possible) is presented in Table 1. Sites listed in Table 1

were surveyed extensively on the ground; under these

conditions, the probability of detection for penguins and

shags approaches 100 % and thus absence in Table 1

should be interpreted as true absence at the time of the

survey. Maps showing the track of the yacht expedition and

all sites are shown in Fig. 1, and maps of the survey sites

requiring further detail are presented in Online Resource 1.

The numbers on the maps correspond to the “Map ID”

numbers on the tables. The distribution of colonies by

species is shown in Online Resource 2. Photodocumenta-

tion of all sites surveyed is available on request; we hope

that our efforts to document these infrequently surveyed

seabird colonies will be useful for future survey work in

this area.

No breeding gentoos were observed south of Cape

Tuxen (site 11 in Table 1 and Online Resource 2). This

represents the most southerly breeding colony for this

species. Comparing our data with the 2010/2011 survey

data reported in Pilipenko (2013), we find that the Cape

Tuxen colony increased in the 2 years separating the sur-

veys. We report on the first complete site censuses of the

three gentoo penguin breeding colonies in the Lemaire

Channel (Glandaz Point, Loubat Point, and Humphries

Heights). Compared with historic data from these sites

(Poncet and Poncet 1987; Woehler 1993), we find that

gentoo populations in the Lemaire Channel are not

declining (cf. Lynch et al. 2012) but rather, like other

gentoo colonies in the Peninsula, are either stable or

increasing in abundance. Table 2 lists the counts of gentoo

penguin colonies by this survey, as well as previous data

that allowed for the estimation of population changes.

Breeding chinstrap penguins were found as far south as

Emperor Island (67°51′S). The breeding pairs found at

Emperor Island, Cone Island and the Islet north east of

Weller Island are recorded here for first time. Chinstrap

penguins were always found in very small groups (mostly

in groups of two breeding pairs, with a maximum of 21

breeding pairs at Point Charcot, Booth Island) or as single

pairs. Table 3 lists the counts of chinstrap penguins for the

sites where they were present.

All colonies of Adelie penguins north of Marguerite

Bay, with the exception of the colonies next to Winkle

Island, declined since the 1980s (Table 4). However, col-

onies in Marguerite Bay did not match this pattern, and

abundances were found to be similar in size or larger than

reported by Poncet and Poncet (1987).

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Table 1 Sites surveyed, describing the status of the colonies if available

Map ID Site Latitude Longitude Gentoo Chinstrap Adelie Blue-eyed shags

1 Pursuit Point (Wiencke I.) −64.905 −63.434 I A A D

2 Truant I. −64.915 −63.411 I A A Pb

3 Loubat Point −65.061 −63.9061 I A A A

4 Humphries Heights −65.065 −64.033 I A A Pb

5 Port Charcot (Booth I.) −65.065 −64.033 I I D Pb

6 Glandaz Point −65.091 −63.957 I A A A

7 Petermann I. −65.167 −64.143 I Pa D Pb

8 Moot Point −65.204 −64.075 I A A A

9 Penguin Point (Galindez I.) −65.248 −64.240 I A A A

10 Yalour Is. −65.254 −64.133 I A D A

11 Cape Tuxen −65.268 −64.124 I A A A

12 Green Island −65.322 −64.153 A A A P

13 Berthelot Is. −65.332 −64.116 A A D A

14 Rocks west of Trundle I. −65.399 −65.300 A Pa P D

15 Jingle Is. −65.438 −65.344 A S D P

16 Weller I. −65.442 −65.364 A A D A

17 Islet southeast of Weller I. −65.451 −65.346 A A D A

18 Smiggers I. −65.459 −65.347 A S D A

19 Islet north east of Fitzkin I. −65.513 −65.479 A A D P

20 Two islets west of Winkle I. −65.519 −65.686 A Pa S P

21 Vieugue I. −65.650 −65.225 A A D A

22 Islets south of Martin I. −65.687 −65.335 A A D P

23 Islet next to Lacktinov I. −65.758 −65.791 A A P P

24 Islets near Armstrong I. −65.889 −66.196 A S D P

25 Fish Is. −66.029 −65.381 A A D I

26 Islet 1 km west of Lavosier I. −66.120 −66.832 A A D P

27 Cape Evensen −66.152 −65.709 A A D A

28 Darbel Is. −66.373 −65.870 A A D P

29 Kuno Point −66.402 −67.168 A A P P

30 Barcroft Is. −66.461 −67.139 A A D P

31 Mist Rocks −66.800 −66.624 A A A P

32 Holdfast Point −66.809 −66.563 A A D P

33 Detaille I. −66.870 −66.786 A A D A

34 Andressen Island (west) −66.874 −66.709 A A D P

35 Andressen Island (east) −66.878 −66.648 A A D P

36 Chatos I. −67.660 −69.152 A A S P

37 Cone I. −67.674 −69.153 A P S P

38 Bongrain Point (Pourquoi Pas I.) −67.722 −67.732 A A I A

39 Ginger I. −67.749 −68.685 A A I I

40 Avian I. −67.769 −68.888 A A S A

41 Emperor I. −67.863 −68.708 A P I P

42 Lagotellerie I. −67.888 −67.379 A A I P

43 Red Rock Ridge −68.291 −67.186 A A I P

I increasing, D decreasing, S stable, A absent, P present—no data available for estimating statusa Intermittently occupied by a single nestb From Lynch et al. (2013)

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123

The distribution of blue-eyed shag colonies follows

closely the distribution of the penguin colonies, sharing

most sites with one or more species of penguins in this

survey (Table 5). Only at Mist Rocks and Green Island

were blue-eyed shags found to be breeding by themselves.

Environmental drivers of Adelie penguin population

change

We find a relationship between the persistence (as fre-

quency across years) of phytoplankton blooms and the

population trajectories of Adelie penguin populations; in

the vicinity of Marguerite Bay, phytoplankton blooms are

more persistent, and Adelie penguin populations have

either maintained their size or grown over the last

30 years, whereas chlorophyll-a poor waters north of

Marguerite Bay with smaller (in spatial extent), less fre-

quent phytoplankton blooms host Adelie penguin

populations that are in decline (Figs. 2, 3). There is a

statistically significant (p \ 0.001) difference in mean

chlorophyll-a between those colonies increasing in abun-

dance and those decreasing in abundance, though it is

important to recognize that the strong spatial autocorre-

lation in both abundance trends and chlorophyll-a make it

difficult to interpret the true statistical significance of this

comparison.

Table 2 Gentoo penguin (Pygoscelis papua) colonies surveyed and references to data collected in previous years by other authors

Map ID Locality Count Accuracy Year Reference

1 Pursuit Point 200 N3/4 1986 Poncet and Poncet (1987)

567 N1 2012 This paper

2 Truant I. 717 C1+ 1986 Poncet and Poncet (1987)


3 and 4 Northern Lemaire (Loubat Point and

Humphries Heights combined)

238 N1 1982 Poncet and Poncet (1987)

237 N1 2010 Pilipenko (2013)


5 Port Charcot (Booth I.) 318 N1 1982 Poncet and Poncet (1987)

1,074 C1 2010 Central Lemaire in Pilipenko (2013)

1,484 N1 2012 This paper

6 Glandaz Point 75 N1 1982 Poncet and Poncet (1987)

115 N1 2010 “Central Lemaire” in Pilipenko (2013)


7 Petermann I. 75 N3 1909 Gain (1914)

480 N3 1971 Muller-Schwarze and Muller-Schwarze (1975)

2,148 N1 2010 Pilipenko (2013)


8 Moot Point 74a N1 2005 Lynch et al. (2013)

389 N1 2010 Pilipenko (2013)


9 Penguin Point (Galindez I.) 93a N1 2008 Lynch et al. (2013)

238 N1 2010 Pilipenko (2013)


10 Yalour Is. 0 N1 1982 Poncet and Poncet (1987)

24a C1 2010 Pilipenko (2013)


11 Cape Tuxen 197a N1 2010 Foothill of Mount Demaria in Pilipenko (2013)


“Year” refers to the year at the beginning of the austral summer (e.g., the survey here reported occurred during the 2012/2013 field season and is

listed as 2012). In most cases, we have restricted Table 2 to counts available from Poncet and Poncet (1987) (or earlier references where

available) and the current survey. Counts from Pilipenko (2013) are also included, where available, as this reference may not be widely available

we would like to clarify how the site names contained therein match up with our current naming scheme. Additional survey counts are available

in Lynch et al. (2013). We have referred to all counts as either nest counts (N), chick counts (C), or adult counts (A), interpreting the intent of the

original survey reports as appropriate, with precision reported as follows: (1) error less than ±5 %, (2) ±5–10 %, (3) ±10–25 %, (4) ±25–50 %a These colonies had never been recorded as existing prior to the survey indicated

Polar Biol

123

Satellite data on sea ice extent show that sea ice con-

centration in the Marguerite Bay area has been declining in

the last 30 years. More importantly, perhaps, the frequency

of years in which the areas surrounding the Marguerite Bay

colonies is free of sea ice in December has increased in the

last 20 years (Fig. 4).

Discussion

Despite a concerted search effort for new gentoo penguin

colonies, we did not find any colonies south of Cape

Tuxen. Our results coincide with the data collected by

Pilipenko (2013), which also confirmed the breeding pop-

ulation at Cape Tuxen. All gentoo colonies for which it was

possible to estimate population change showed a signifi-

cant increase in their breeding abundance, consistent with

the general trend of gentoo penguin population growth

along the WAP (Lynch et al. 2012).

Despite widespread population declines along most of

the WAP, we found that small numbers of chinstrap pen-

guins south of 65°S have persisted (Table 3). We report

here for the first time chinstrap penguins breeding in small

numbers as far south as Cone Island and Emperor Island,

the latter of which may now be the southern-most breeding

population [given the apparent disappearance of the colony

at Peter I Island; see Woehler (1993)]. There are significant

environmental and sea ice phenology differences between

these southern-most chinstrap occupied islands and the

South Sandwich Islands where chinstrap penguins are most

abundant. It remains to be seen whether these southern

WAP chinstrap penguins differ from their more northern

conspecifics with respect to breeding phenology, migration

strategy, or foraging strategies. While chinstrap penguins

are apparently able to successfully breed along the southern

WAP, the biotic and abiotic constraints on greater expan-

sion of chinstrap colonization and persistence remain an

open question. We speculate that the rates of extinction for

these small, isolated groups [as well as on other extremely

isolated islands such as Peter I Island, Heard Island, and the

Balleny Islands; see Woehler (1993)], would be high

absent at least occasional migration from more abundant

populations at the core of their breeding range, but the rates

of these processes are unknown. Given the lack of physi-

ological (or obvious ecological) barriers for breeding this

far south, it is not clear why chinstraps are not more

abundant in this region.

Relatively little is known about the abundance and

distribution of blue-eyed shags in the area covered by this

survey, and we have only sparse historical data for these

populations to assess how the population might have

changed in the last few decades. At two of the more

Table 3 Chinstrap penguin (Pygoscelis antarctica) colonies surveyed and references to data collected in previous years by other authors


5 Port Charcot (Booth I.) 3 C1 1982 Poncet and Poncet (1987)

21 N1 2010 Pilipenko (2013)


7 Petermann I. 1 N1 2010 Pilipenko (2013)


14 Rocks west of Trundle I. 1 N1 2012 This paper

15 and 18 Pitt Is. North (Jingle I. and

Smiggers I. combined)

0 N1 1983 Poncet and Poncet (1987)


20 Two islets next to Winkle I. 0 N1 1982 Pitt Islands South in Poncet and Poncet (1987)


24 Islets near Armstrong I. 1 N1 1983 Poncet and Poncet (1987)

6 N1 1990 Woehler (1993)


37 Cone I. 2 N1 2012 This paper

41 Emperor I. 1 N1 2012 This paper

“Year” refers to the year at the beginning of the austral summer (e.g., the survey here reported occurred during the 2012/2013 field season and is

listed as 2012). In most cases, we have restricted Table 2 to counts available from Poncet and Poncet (1987) (or earlier references where

available) and the current survey. Counts from Pilipenko (2013) are also included, where available, as this reference may not be widely available

we would like to clarify how the site names contained therein match up with our current naming scheme. Additional survey counts are available

in Lynch et al. (2013). We have referred to all counts as either nest counts (N), chick counts (C), or adult counts (A), interpreting the intent of the

original survey reports as appropriate, with precision reported as follows: (1) error less than ±5 %, (2) ±5–10 %, (3) ±10–25 %, (4) ±25–50 %

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Table 4 Adelie penguin (Pygoscelis adeliae) colonies surveyed and references to data collected in previous years by other authors


5 Port Charcot (Booth I.) 500 A5 1909 Croxall and Kirkwood (1979)

83 C1 1982 Poncet and Poncet (1987)

9 C1 2010 Pilipenko (2013)


7 Petermann I. 925 A3 1909 Croxall and Kirkwood (1979)

1,540 N3 1971 Muller-Schwarze and Muller-Schwarze (1975)

987 N1 1982 Airey (1982), in Poncet and Poncet (1987)

251 N1 2010 Pilipenko (2013)


10 Yalour Is. 10,400 N1, N3 1958 Croxall and Kirkwood (1979)

5,865 N1 1982 Airey (1982), in Poncet and Poncet (1987)

2,555 N1 2010 Pilipenko (2013)


13 Berthelot Is. 904 N1 1982 Airey (1982), in Poncet and Poncet (1987)

346 N1 2010 Pilipenko (2013)


14 Rocks west of Trundle I. 347 N1 2012 This paper

15, 16, 17 and 18 Pitt Is. North (Jingle I., Weller I.,

Islet southeast of Weller I., and

Smiggers I. combined)

3,424 + 350 C1 + N3/4 1983 Poncet and Poncet (1987)


19 Islet north east of Fitzkin I. 250 N3/4 1983 Poncet and Poncet (1987)


20 Two islets next to Winkle I. 52 C1 1982 Pitt Is. south in Poncet and Poncet (1987)


21 Vieugue I. 600 N4 1986 Poncet and Poncet (1987)


22 Islets south of Martin I. 1,277 C1 1982 “Kim Is.” in Poncet and Poncet (1987)


23 Islet next to Lacktinov I. 38 N1 2012 This paper

24 Islets near Armstrong I. 9,626 + 700 C1 + N 3/4 1983 Poncet and Poncet (1987)

2,813 C1 2012 This paper

25 Fish Is. 4,000 N3/4 1983 Poncet and Poncet (1987)


26 Islet 1 km west of Lavosier I. 150 N4/5 1986 Poncet and Poncet (1987)


27 Cape Evensen (including

penguins on offshore rocks)

1,200 N3/4 1983 Poncet and Poncet (1987)

1,100 N3/4 1990 Woehler (1993)


28 Darbel Islands 650 N3/4 1983 Poncet and Poncet (1987)


29 Kuno Point 235 N1 2012 This paper

30 Barcroft Is. 1,600 N4/5 1982 Poncet and Poncet (1987)


32 Holdfast Point 625 N3/4 1983 Poncet and Poncet (1987)


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northern sites in our survey area (Pursuit Point and Rocks

west of Trundle Island), shag populations appear to be

decreasing, while at two of the sites further south (Fish

Islands and Ginger Island), they appear to be stable or even

increasing. This pattern is consistent with the general

north–south trend seen for Adelie penguins, though con-

tinued observation of blue-eyed shag populations will be

required to understand their dynamics in the context of

underlying environmental conditions. Using the estimated

global population of 10,900 breeding pairs by Orta (1992)

as reported by Casaux and Barrera-Oro (2006), our survey

covered approximately 25 % of the global population of

Phalacrocorax (atriceps) bransfieldensis.

Primary productivity strongly correlated with trends

in Adelie abundance

Persistent phytoplankton blooms in Marguerite Bay are

congruent with population numbers for Adelie populations

that are stable or increasing, suggesting a relationship

between persistent primary productivity and maintenance

of Adelie populations. Referencing previous surveys in this

region (Poncet and Poncet 1987; Woehler 1993) and the

analyses reported in Lynch et al. (2012), it is clear that all

Adelie populations from the Yalour Islands south to Mar-

guerite Bay have declined, some by as much as 75 %. By

contrast, the Adelie populations at eight open-ocean-facing

Table 4 continued


33 Detaille I. 10,000 A5 1908 Croxall and Kirkwood (1979)

350 N3 1957 Croxall and Kirkwood (1979)

858 C1 1985 Poncet and Poncet (1987)

561 C1 2012 This paper

34 Andresen I. (northwest coast) 2,200 B3/4 1983 Poncet and Poncet (1987)


35 Andresen I. (northeast coast) 281 N1 2012 This paper

36 Chatos I. 100 N4/5 1982 Poncet and Poncet (1987)


37 Cone I. 3,000 N4/5 1982 Poncet and Poncet (1987)


38 Bongrain Point (Pourquoi Pas I.) 700 N3/4 1983 Poncet and Poncet (1987)


39 Ginger I. 2,790 C1, C3 1982 Poncet and Poncet (1987)


40 Avian I. 25,000 A4 1968 Croxall and Kirkwood (1979)

35,600 N2 1978 Poncet and Poncet (1987)

77,515a N (unknown

precision)

2012 Sailley et al. (2013)


41 Emperor I. 700 N4/5 1985 Poncet and Poncet (1987)


42 Lagotellerie I. 400 N3 1936 Croxall and Kirkwood (1979)

2,402 N1 1955 Croxall and Kirkwood (1979)

1,000 N3 1960 Croxall and Kirkwood (1979)

1,720 C1 1982 Poncet and Poncet (1987)


43 Red Rock Ridge 540 N3 1936 Croxall and Kirkwood (1979)

900 N3 1960 Croxall and Kirkwood (1979)

1,820 C1 1983 Poncet and Poncet (1987)


A complete list of abundance estimates for many of these sites may be found in Lynch et al. (2013). We have referred to all counts as either nest

counts (N), chick counts (C), or adult counts (A), interpreting the intent of the original survey reports as appropriate, with precision reported as

follows: (1) error less than ±5 %, (2) ±5–10 %, (3) ±10–25 %, (4) ±25–50 %a There is a significant disparity between two surveys of Avian Island in 2013; it is not clear whether the difference stems from differing survey

targets (nests vs. chicks), a massive loss in the number of chicks between the two surveys, or another unidentified difference in survey protocols

Polar Biol

123

sites in Marguerite Bay (Chatos Island, Cono Island, Gin-

ger Islands, Bongrain Point at Pourquois-Pas Island, Red

Rock Ridge, Lagotellerie Island, Emperor Island, and

Avian Island) appear to be maintaining their size or

increasing, consistent with other research suggesting that

northern Marguerite Bay is a biological “hotspot” with

high occurrence rates of krill predators (Friedlaender et al.

2011).

The Marguerite Bay area is of particular interest because

it has unique oceanographic characteristics (e.g., Schofield

et al. 2013) and frequently hosts the largest and most

persistent phytoplankton blooms on the WAP (Marrari

et al. 2008). Spring and summer phytoplankton blooms are

an important factor influencing Antarctic krill (Euphausiasuperba) recruitment in the Antarctic Peninsula region

(Marrari et al. 2008), which is widely recognized as a

major link between primary producers and many popula-

tions of krill-feeding vertebrates, including penguins

(Ballerini et al. 2014). It has been shown that there is an

alongshore gradient of phytoplankton biomass in the

Table 5 Blue-eyed shag (Phalacrocorax [atriceps] bransfieldensis) colonies surveyed


1 Pursuit Point 140 Unknown 1986 Harris et al. (2011)


12 Green I. 89 N1 2012 This paper

14 Rocks west of Trundle I. 140 Unknown 1989 Harris et al. (2011)


15 Jingle Is. 7 N1 2012 This paper

19 Islet north east of Fitzkin I. 40 N1 2012 This paper

20 Two islets west of Winkle I. 38 N1 2012 This paper

22 Islets south of Martin I. 24 N1 2007 Lynch et al. (2013)


23 Islet next to Lacktinov I. 60 N1 2012 This paper

24 Islets near Armstrong I. 114 N1 2012 This paper

25 Fish Is. 78 C1 1994 Lynch et al. (2013)

31 N1 2002 Lynch et al. (2013)

55 N1 2007 Lynch et al. (2013)

137 C1 2007 Lynch et al. (2013)

65 C1 2008 Lynch et al. (2013)


26 Islet 1 km west of Lavosier I. 39 N1 2012 This paper

28 Darbel Is. 39 N1 2012 This paper

29 Kuno Point 15 N1 2012 This paper

30 Barcroft Is. 277 N1 2012 This paper

31 Mist Rocks 17 N1 2012 This paper

32 Holdfast Point 45 N1 2012 This paper

34 and 35 Andressen I. 30 N1 2012 This paper

36 Chatos I. 10 N1 2012 This paper

37 Cone I. 130 N1 2012 This paper

39 Ginger I. 275 Unknown 1980s Harris et al. (2011)


41 Emperor I. 810 N1 2012 This paper

42 Lagotellerie I. 270 N1 2012 This paper

43 Red Rock Ridge 3 N1 2007 Lynch et al. (2013)

19 C1 2009 Lynch et al. (2013)

9 C1 2012 This paper

A complete list of abundance estimates for many of these sites may be found in Lynch et al. (2013). Green Island was surveyed from an offshore

zodiac. We have referred to all counts as either nest counts (N), chick counts (C), or adult counts (A), interpreting the intent of the original survey

reports as appropriate, with precision reported as follows: (1) error less than ±5 %, (2) ±5–10 %, (3) ±10–25 %, (4) ±25–50 %

Polar Biol

123

northern part of the Antarctic Peninsula, with higher bio-

mass in the northern sectors earlier in the productive

season, which later progresses to the southeast as the sea

ice retreats (Smith et al. 1998; Garibotti et al. 2003). In this

area, intermediate values of chlorophyll-a were observed

(0.1–2 mg/m3) with small spatial extent, short-lived blooms

(chlorophyll values greater than 2 mg/m3 in some near

shore regions, Marrari et al. 2008). However, the Mar-

guerite Bay area showed persistently high chlorophyll

concentrations (0.1–47 mg/m3) during spring and summer

in comparison with any other sector west of the Antarctic

Peninsula (Marrari et al. 2008). Reports on chlorophyll-aconcentrations in the Marguerite Bay area vary from

2.30 mg/m3 (Arrigo and van Dijken 2003) to up to 17.86

DecreasingIncreasing

No changeNo data

201120102009

200820072006

200520042003

Low High

Chlorophyll-a concentration

A

B

N

Fig. 2 Adelie penguin

population trends along with the

distribution of chlorophyll-aconcentration (available from:

http://oceancolor.gsfc.nasa.

gov). The dotted line indicates

the approximate location of the

transition zone described in the

text. Note that the color scale is

a stretched scale based on stan-

dard deviation and is therefore

not a linear representation of

relative chlorophyll-a values.

a Mean January chlorophyll-aconcentration (2003–2014),

b mean January chlorophyll-aconcentration for each year

from 2003 to 2011. Note the

persistence of the phytoplankton

blooms in the Marguerite Bay

area

Polar Biol

123

and 25 mg/m3 (Garibotti et al. 2003; Meyer et al. 2003,

respectively).

It is interesting to compare our findings with Montes-

Hugo et al. (2009), who find an unambiguous demarcation

between areas of decreasing chlorophyll-a (northern WAP)

and increasing chlorophyll-a (southern WAP). At the

broadest scale, our findings are consistent with this picture.

However, Montes-Hugo et al. (2009) found that chloro-

phyll-a has increased 66 % on average from 1978–1986 to

1998–2006 between Marguerite Bay and south of Anvers

Island (63.8°–67.8°S, 64.4°–73.0°W)—an area where

Adelie penguin populations have been declining in the last

decades. We propose two possible explanations for this

paradox. One is suggested by the fact that the increase in

chlorophyll-a in this region is driven by high chlorophyll

values during only 2 years, and it may be that a change in

the frequency of years with persistently high concentration

in the phytoplankton blooms over time may be more rel-

evant to penguin population trends than an average trend

on phytoplankton concentration skewed by infrequent high

blooms (cf. Fraser and Hofmann 2003). It may also be the

case that this ecological boundary continues to move

southward, so the line between increasing and decreasing

chlorophyll-a concentrations may have shifted further

south since 2006 [the last year included in the analysis by

Montes-Hugo et al. (2009)].

Summer sea ice declines improves colony access

In the last 30 years, summer sea ice extent has been

declining in Marguerite Bay (Fig. 4). Our analysis of

summer sea ice in the proximities of penguin colonies

showed that summer sea ice has declined at all sites,

especially since the late 1980s. The Marguerite Bay area

has essentially shifted from a regime of extensive summer

sea ice to less extensive summer sea ice, including years

with no summer sea ice (Fig. 4). Several studies have

highlighted that in breeding seasons with reduced summer

sea ice adjacent to rookeries Adelie penguins are able to

use fat reserves and food for breeding purposes (egg pro-

duction, courtship, incubation and chick feeding) instead of

using those resources for traveling to reach open water (at

Cape Royds, Stonehouse 1963; at Cape Crozier, Ainley and

Leresche 1973; in the Ross Sea area, Taylor et al. 1990).

Highlighting the potentially negative consequences of

heavy summer sea ice, Croxall and Kirkwood (1979) noted

that during the 1958–1959 breeding season in Detaille

Island, penguins had to walk nearly 50 km to reach open

water, which led to almost complete nest failure in that

year.

Our survey data suggest that Adelie penguin populations

flourish where persistently high primary productivity

occurs in areas without extensive summer sea ice that

might block access to the colony during the austral spring.

In areas north of Marguerite Bay, loss of sea ice has

increased access to the colony for breeding but at the

expense of reduced food availability for krill specialist

predators (Trivelpiece et al. 2011). We believe that Mar-

guerite Bay benefits from consistently high primary

productivity, in part due to its unique hydrogeography

(Ashjian et al. 2004), and this mitigates regional losses of

krill habitat due to declining annual sea ice cover. At the

No data Decreasing No change Increasing

0.8

1.0

1.2

1.4

1.6

1.8

Change in Adelie penguin colony abundance

chlo

roph

yll -

a (m

g/m

)3

Difference in group means

Freq

uenc

y

−0.2 0.0 0.2 0.4

5010

015

0data

permuted0

Fig. 3 Box plot showing January chlorophyll-a concentration (avail-

able from: http://oceancolor.gsfc.nasa.gov) around the colonies

grouped by the population status of the colonies. Boxes extend to the

first and third quartiles and whiskers extend to the extrema

(points[1.5 times the inter-quartile range from the box represented

by circles). Inset mean difference between the “increasing” and

“decreasing” group means under random permutation of the group

labels (n = 999). Arrow indicates the empirical difference in group

means, which is larger than any of the 999 random permutations

(hence, p\ 0.001)

Min

imum

sea

−ice

con

cent

ratio

n (%

)

1980 1985 1990 1995 2000 2005 2010

C

Year

0

40

80

1980 1985 1990 1995 2000 2005 2010

B

0

40

80

1980 1985 1990 1995 2000 2005 2010

A

0

40

80 p = 0.02R = 0.14

p = 0.003R = 0.23

p < 0.001R = 0.28

2

2

2

Fig. 4 Minimum sea ice concentration for December around the

Marguerite Bay colonies. (Sea ice data available from the National

Snow and Ice Data Center: http://nsidc.org/). a Cone Island and

Chatos Island; b Avian Island, Ginger Island and Emperor Island; and

c Bongrain Point (Pourquoi Pas Island), Lagotellerie Island and Red

Rock Ridge. The dotted line shows the general trend of sea ice con-

centration for the sites

Polar Biol

123

same time, decreasing sea ice is likely allowing Adelie

penguins to recoup any reduction in prey availability by

reductions in net reproductive energy, with reduced for-

aging effort and greater efficiencies due to access to open

water. It is possible that continued reduction in sea ice will

exceed the threshold where the net benefit of access to the

colony is outweighed by concomitant loss of prey.

While the biggest gains in Adelie penguin abundance in

the Marguerite Bay area have occurred between the mid-

1980s and the 2012/2013 season, it is interesting to note

that these populations have been increasing at least since

the 1940s. For example, Croxall and Kirkwood (1979)

noted that “a real increase in numbers [at Lagotellerie

Island] had taken place by the late 1940s–early 1950s”.

Therefore, while recent gains in abundance may be

explained by improving sea ice conditions (from the per-

spective of access to breeding colonies), increases earlier in

the twentieth century prior to increasing air temperatures

and declining sea ice (King and Turner 1997; Smith and

Stammerjohn 2001) are not easily explained by abiotic

drivers. These increases may reflect a response to har-

vesting of other krill predators (e.g., seals and whales), as

reviewed by Ainley et al. (2009), though the data on pen-

guin abundance we have for this region are insufficient to

make any firm conclusions in this regard.

While logistical difficulties in accessing the southern

portion of the WAP make it difficult to census these pop-

ulations regularly, it is clear that Marguerite Bay and areas

just north are not just static “predator hotspots” but rep-

resent the leading edge of climatic changes that can bring

transient benefits to species such as penguins. Whether

Marguerite Bay will remain a refugium for Adelie pen-

guins on the WAP in the long term remains to be seen, but

clearly this is a region deserving of focused attention over

the next several decades.

Acknowledgments We gratefully acknowledge the support of The

Tinker Foundation, whose support enabled Oceanites, Inc. and the

Antarctic Site Inventory team to charter Golden Fleece for this

directed research, and in addition, thank the U.S. National Science

Foundation Office of Polar Programs and Geography and Spatial

Sciences (Awards Nos. 07-39515 and 12-55058). We also acknowl-

edge the support of NASA headquarters under the NASA Earth and

Space Fellowship Program—Grant NNX10AN55H to P. C. We are

grateful to the crew of the yacht Golden Fleece, Yoann Gourdet and

Cathy Colle, for ensuring the safety and well-being of the Antarctic

Site Inventory research team during their work period in the Antarctic

Peninsula. Cheesemans’ Ecology Safaris and One Ocean Expeditions,

which graciously provided transportation to and from the Peninsula.

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