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A Comprehensive Coastal Seabird Survey Maps out the Front Lines of Ecological Change on the Western Antarctic Peninsula

A Comprehensive Coastal Seabird Survey Maps out the Front Lines of Ecological Change on the Western Antarctic Peninsula

Polar Biol DOI 10.1007/s00300-015-1651-x

ORIGINAL PAPER

A comprehensive coastal seabird survey maps out the front lines of ecological change on the western

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 different ocean dynamics than in areas just outside Mar- are known to be shifting in abundance and distribution in guerite Bay, has maintained persistent phytoplankton response to changing sea ice and prey distributions, but the blooms over the past decade even as summer sea ice extent, spatial extent of these changes has remained an open which can inhibit access to breeding areas, has declined. question because survey efforts have focused on the more This provides further support for the hypothesis that ocean easily accessed northern coastline. We used a yacht-based productivity and sea ice dynamics are critical factors reg- field expedition (January 5–21, 2013) to complete the first ulating Ade´lie penguin abundance in the region and that comprehensive penguin (Pygoscelis spp.) and blue-eyed is now at the front lines of ecological shag (Phalacrocorax [atriceps] bransfieldensis) population change in this region. survey of the Graham and Loubet Coasts of the western Antarctic Peninsula since the mid-1980s. Our surveys Keywords Penguins · Blue-eyed shag · Marguerite document a sharp transition zone at the northern boundary Bay · Sea ice · Phytoplankton blooms of Marguerite Bay; north of this boundary zone, we con- firm widespread declines in Ade´lie penguins and increasing populations of gentoo penguins, but south of this zone we Introduction find Ade´lie populations that have remained stable or increased in abundance since the previous surveys by It is now well established that penguin populations on the Poncet and Poncet (Br Antarct Surv Bull 77:109–129, Antarctic Peninsula have been changing over the past three 1987). Marguerite Bay has long been known as a predator decades (Trivelpiece et al. 2011; Lynch et al. 2012; “hotspot,” but our findings suggest that Marguerite Bay has Ducklow et al. 2013). Particular attention has focused on actually been improving for marine predators for at least widespread declines in the abundance of Ade´lie penguin several decades. Marguerite Bay, which has fundamentally (Pygoscelis adeliae) colonies situated along the western coast of the Antarctic Peninsula (Lynch et al. 2012; Lynch Electronic supplementary material The online version of this and LaRue 2014), as well as increasing abundance and article (doi:10.1007/s00300-015-1651-x) contains supplementary southward expansion of gentoo penguins (P. papua) (Lynch material, which is available to authorized users. et al. 2012). Evidence suggests that environmental factors P. Casanovas · R. Naveen · S. Forrest associated with climate change, such as declining sea ice Oceanites, Inc., Chevy Chase, MD, USA and shifts in primary productivity, play a significant role in these shifting patterns of abundance and distribution (Fra- J. Poncet Golden Fleece Expedition Cruises, Beaver Island, ser et al. 1992; Smith et al. 1999; Croxall et al. 2002; Falkland Islands Clarke et al. 2007; Murphy et al. 2007; Trivelpiece et al. 2011). Most studies to date, however, have focused on & H. J. Lynch ( ) colonies north of 65°S, and thus information on population Ecology and Evolution Department, Stony Brook University, ° Stony Brook, NY 11794, USA changes south of 65 S and in the vicinity of Marguerite e-mail: [email protected] Bay has been limited. The survey work reported by Poncet 123 Polar Biol and Poncet (1987), who censused penguin colonies in this locations due to dispersal of individuals over small island region from 1983 to 1987, is the only comprehensive field archipelagos or islands separated from the mainland. Ide- survey of the region prior to that reported here. Their data ally, each “site” encompasses a single breeding population, provide the baseline against which we can assess changes but we have defined their boundaries and naming schema in the abundance and distribution of penguins breeding to remain consistent with historical precedent. Mild south of 65°S on the western Antarctic Peninsula (WAP). weather conditions and the absence of pack ice facilitated Monitoring seabird populations in the Antarctic is the work, allowing for surveying every day and access to important because changes in their abundance and distri- all targeted sites. We surveyed all of the known breeding bution may indicate regional climate change (Croxall et al. locations described in Poncet and Poncet (1987) south of 2002) or direct or indirect human disturbance (e.g., tour- Moot Point except for Island (69°40′S, 68°47′W), ism, marine traffic, commercial harvesting of marine which could not be reached because of time/ice constraints resources). However, limited data south of 65°S have made and distance. The survey occurred after the peak of pen- it impossible to know whether observed changes persist guin egg-laying (for nest counts) and before the peak of south of the latitudinal range for which data have been penguin chick-cre´ching (for chick counts). We mapped, available. Lynch et al. (2012) found that while Ade´lie through waypoints and tracklogs as appropriate, all sur- penguins were declining over most of the western Antarctic veyed sites, as well as the Golden Fleece’s route. Peninsula (WAP), populations at Bongrain Point, Pourquoi We systematically searched all known or discovered Pas Island (−67.72°, −67.73°) and Red Rock Ridge islands, islets, and penguin/shag colonies thereon, relying (–68.29°, −67.18°) were actually increasing. At the same upon Capt. Je´roˆme Poncet’s [30 years experience navi- time, gentoo penguins were found to be expanding their gating these waters and on his navigation notes from the range further south, prompting Lynch et al. (2012)to surveys described in Poncet and Poncet (1987). With the predict further expansion south to the Berthelot Islands. exception of the shag survey at Green Island, all of our More recent evidence suggests that chinstrap penguins (P. surveys were accomplished by researchers (PC, RN, and ), which are declining regionally (e.g., Lynch SF) on land, proceeding from Golden Fleece to shore by et al. 2012), may also be establishing new colonies at their zodiac. All encountered colonies of gentoo penguins, southern range margin (~65°S), although only in areas chinstrap penguins, Ade´lie penguins, and blue-eyed shags already occupied by other pygoscelid penguins (Lynch were mapped and censused by direct enumeration of et al. 2013). To address these open questions, we organized individual occupied nests or chicks [see Lynch et al. (2008) a multipronged survey of the Graham and Loubet Coasts for details on survey methodology]. We counted nests or (between 65° and 68° South, including the Marguerite Bay chicks individually three times and report the average of area) using a comprehensive yacht-based field survey of those three counts; estimates of abundance are, except as the region supported by a coastal survey of high-resolution noted, accurate to ±5 %. We focused our survey on pen- satellite imagery. While most of the WAP is being moni- guin breeding sites reported by Poncet and Poncet (1987) tored regularly (Lynch et al. 2013), the area south of 65°S and the Wildlife Awareness Manual (Harris 2006), as well is not routinely visited by passenger vessels. Small yacht as at locations that had been determined by remotely operations allow for the surveying of areas that are extre- sensed data to potentially contain rookeries. mely difficult or impossible to reach by bigger vessels and Gentoo penguins were counted at eight census sites. All provide greater flexibility for scheduling travel among gentoo penguins were past the peak of egg-laying, many sites. brooding 1–2 week old chicks, and no cre´ching was observed. In this circumstance, the focus throughout was on obtaining nest counts. Chinstrap penguins were cens- Methods used at seven locations and found breeding in small numbers. Only nests with eggs or 1–2 week old chicks Field survey were observed, and thus, the focus was nest counts. Ade´lie penguins were censused at 31 census sites. Ade´lies were From January 5 to 21, 2013, we used the yacht Golden past the peak of egg-laying, with many chicks already Fleece (with a 19.5 m steel hull, a beam of 6.19 m, and a hatched (mostly 2–4 weeks of age) but not yet starting to maximum draft of 2.48 m) to survey the WAP coastline cre`che, so we focused on nest counts. However, at five sites between 65°06′ and 68°18′S, including offshore islands in in Marguerite Bay (Red Rock Ridge, , the Grandidier Channel, Crystal Sound, the west and , Chatos Island, and Cone Island), a significant southern coast of , and the islands in proportion of the colony had cre´ched and we counted Marguerite Bay (Fig. 1). Over this period, we completed 43 chicks instead of occupied nests. Where it was possible to site censuses, where some sites included multiple census do so, both occupied nests and chicks were simultaneously 123 Polar Biol

Fig. 1 Track of the Golden 180o W Fleece route representing the o 60 o S o area searched and surveyed for 30 W 30 W this study. Areas along this track not reported in this paper represent true absence within 70 o S o the detection limits of the 60 W 60o W survey (up to 5 km). a Gerlache Strait area, b Lemaire Channel 80 o S to Green Island area, c Renaud Island area, d Crystal Sound area, e Marguerite Bay area. The numbers on the maps 90 o W 90 o E correspond to the Map ID numbers in Table 1. All imagery Copyright (2014) by Digital Globe, Inc.

o 120o W 120 E

o 150o W 150 E

180o W A B

2 3 1 4 6 A 5 048 km B 8 7 10 11 13 C 07.5 15 km 9 12 o

65 S C 14 15 17 D 18 21 16 19 22 20

E 23 25

o 27

66 S 24 28 0 70 140 km 0 25 50 km

D E

26 42 38 43 32 31 35 29 30 34 33

39 41 36 40 37 0 20 40 km 0 30 60 km

123 Polar Biol censused. We also surveyed all blue-eyed shag (Phala- Results crocorax [atriceps] bransfieldensis) nests in the region. Data collected by Poncet and Poncet (1987) were similar Field survey in methodology, though the earlier survey included some estimates obtained from offshore aboard a yacht as The list of sites visited along with the presence–absence reflected in their lower precision. Our assessment of pop- summary for each site (describing the status of the colony ulation change is based on all the available data for each if possible) is presented in Table 1. Sites listed in Table 1 site surveyed, including data from Poncet and Poncet were surveyed extensively on the ground; under these (1987), the Antarctic Site Inventory database (Naveen and conditions, the probability of detection for penguins and Lynch 2011), and other published sources. shags approaches 100 % and thus absence in Table 1 should be interpreted as true absence at the time of the Environmental drivers of Ade´lie population change survey. Maps showing the track of the yacht expedition and all sites are shown in Fig. 1, and maps of the survey sites We analyzed changes in penguin abundance in the context of requiring further detail are presented in Online Resource 1. the oceanographic characteristics of the study area, in par- The numbers on the maps correspond to the “Map ID” ticular the patterns of phytoplankton blooms and summer sea numbers on the tables. The distribution of colonies by ice extent. Phytoplankton blooms were quantified using the species is shown in Online Resource 2. Photodocumenta- merged satellite measurements of ocean chlorophyll-a data tion of all sites surveyed is available on request; we hope derived from the moderate resolution imaging spectroradi- that our efforts to document these infrequently surveyed ometer (MODIS), in orbit on the Aqua platform, and the Sea- seabird colonies will be useful for future survey work in viewing Wide Field-of-View Sensor (SeaWIFS), in orbit on this area. the OrbView-2. We used the level 3 monthly merged chlo- No breeding gentoos were observed south of rophyll product (concentration of chlorophyll-a in mg/m3), Tuxen (site 11 in Table 1 and Online Resource 2). This with a spatial resolution of 9 km2. The data were obtained represents the most southerly breeding colony for this from the Ocean Biology Processing Group (OBPG), Global species. Comparing our data with the 2010/2011 survey Change Data Center, Earth Sciences Division, Science and data reported in Pilipenko (2013), we find that the Cape Exploration Directorate, Goddard Space Flight Center, Tuxen colony increased in the 2 years separating the sur- NASA (http://oceancolor.gsfc.nasa.gov) in hierarchical data veys. We report on the first complete site censuses of the format and converted to ASCII format using ESRI Arc- three gentoo penguin breeding colonies in the Lemaire GIS10.0. We traced a circular buffer around each colony, Channel (Glandaz Point, Loubat Point, and Humphries with radius (50 km) equal to the maximum Ade´lie foraging Heights). Compared with historic data from these sites distance (Trivelpiece et al. 1987). We calculated the mean (Poncet and Poncet 1987; Woehler 1993), we find that values for chlorophyll-a concentration over a period of gentoo populations in the Lemaire Channel are not 10 years for the month of January, in the over-water portion declining (cf. Lynch et al. 2012) but rather, like other of the buffer. Due to small sample size and non-normality gentoo colonies in the Peninsula, are either stable or in the within-group distribution of chlorophyll-a concen- increasing in abundance. Table 2 lists the counts of gentoo tration, differences between Ade´lie penguin colonies penguin colonies by this survey, as well as previous data increasing in abundance and decreasing in abundance were that allowed for the estimation of population changes. assessed using a permutation test (n = 999 random permu- Breeding chinstrap penguins were found as far south as tations of the values between the “increasing” and (67°51′S). The breeding pairs found at “decreasing” categories). Emperor Island, Cone Island and the Islet north east of Sea ice spatiotemporal distribution was estimated from Weller Island are recorded here for first time. Chinstrap NIMBUS-7 Scanning Multichannel Microwave Radiome- penguins were always found in very small groups (mostly ter (SMMR) and the Defense Meteorological Satellite in groups of two breeding pairs, with a maximum of 21 Programs (DMSP) Special Sensor Microwave/Imager breeding pairs at Point Charcot, Booth Island) or as single (SSM/I) and the Special Sensor Microwave Imager/Soun- pairs. Table 3 lists the counts of chinstrap penguins for the der (SSMIS) passive microwave data (25 km2 spatial sites where they were present. resolution). The data were obtained from the National All colonies of Ade´lie penguins north of Marguerite Snow and Ice Data Center in raw binary format and con- Bay, with the exception of the colonies next to Winkle verted to ASCII format using ESRI ArcGIS 10.0. We Island, declined since the 1980s (Table 4). However, col- calculated the minimum sea ice concentration for the onies in Marguerite Bay did not match this pattern, and month of December for the same buffers described above abundances were found to be similar in size or larger than from 1978 to 2011. reported by Poncet and Poncet (1987). 123 Polar Biol

Table 1 Sites surveyed, describing the status of the colonies if available Map ID Site Latitude Longitude Gentoo Chinstrap Ade´lie 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 DPb 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 PD 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 SP 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 status a Intermittently occupied by a single nest b From Lynch et al. (2013)

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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) 921 N1 2012 This paper 3 and 4 Northern Lemaire (Loubat Point and 238 N1 1982 Poncet and Poncet (1987) Humphries Heights combined) 237 N1 2010 Pilipenko (2013) 626 N1 2012 This paper 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) 145 N1 2012 This paper 7 Petermann I. 75 N3 1909 Gain (1914) 480 N3 1971 Mu¨ller-Schwarze and Mu¨ller-Schwarze (1975) 2,148 N1 2010 Pilipenko (2013) 3,300 N1 2012 This paper 8 Moot Point 74a N1 2005 Lynch et al. (2013) 389 N1 2010 Pilipenko (2013) 479 N1 2012 This paper 9 Penguin Point (Galindez I.) 93a N1 2008 Lynch et al. (2013) 238 N1 2010 Pilipenko (2013) 273 N1 2012 This paper 10 Yalour Is. 0 N1 1982 Poncet and Poncet (1987) 24a C1 2010 Pilipenko (2013) 28 N1 2012 This paper 11 Cape Tuxen 197a N1 2010 Foothill of Mount Demaria in Pilipenko (2013) 282 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 % a These colonies had never been recorded as existing prior to the survey indicated

The distribution of blue-eyed shag colonies follows more persistent, and Ade´lie penguin populations have closely the distribution of the penguin colonies, sharing either maintained their size or grown over the last most sites with one or more species of penguins in this 30 years, whereas chlorophyll-a poor waters north of survey (Table 5). Only at Mist Rocks and Green Island Marguerite Bay with smaller (in spatial extent), less fre- were blue-eyed shags found to be breeding by themselves. quent phytoplankton blooms host Ade´lie penguin populations that are in decline (Figs. 2, 3). There is a Environmental drivers of Ade´lie penguin population statistically significant (p \ 0.001) difference in mean change chlorophyll-a between those colonies increasing in abun- dance and those decreasing in abundance, though it is We find a relationship between the persistence (as fre- important to recognize that the strong spatial autocorre- quency across years) of phytoplankton blooms and the lation in both abundance trends and chlorophyll-a make it population trajectories of Ade´lie penguin populations; in difficult to interpret the true statistical significance of this the vicinity of Marguerite Bay, phytoplankton blooms are comparison.

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Table 3 Chinstrap penguin (Pygoscelis antarctica) colonies surveyed and references to data collected in previous years by other authors Map ID Locality Count Accuracy Year Reference

5 Port Charcot (Booth I.) 3 C1 1982 Poncet and Poncet (1987) 21 N1 2010 Pilipenko (2013) 22 N1 2012 This paper 7 Petermann I. 1 N1 2010 Pilipenko (2013) 0 N1 2012 This paper 14 Rocks west of Trundle I. 1 N1 2012 This paper 15 and 18 Pitt Is. North (Jingle I. and 0 N1 1983 Poncet and Poncet (1987) Smiggers I. combined) 4 N1 2012 This paper 20 Two islets next to Winkle I. 0 N1 1982 Pitt Islands South in Poncet and Poncet (1987) 1 N1 2012 This paper 24 Islets near Armstrong I. 1 N1 1983 Poncet and Poncet (1987) 6 N1 1990 Woehler (1993) 1 N1 2012 This paper 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 %

Satellite data on sea ice extent show that sea ice con- at Peter I Island; see Woehler (1993)]. There are significant centration in the Marguerite Bay area has been declining in environmental and sea ice phenology differences between the last 30 years. More importantly, perhaps, the frequency these southern-most chinstrap occupied islands and the of years in which the areas surrounding the Marguerite Bay South Sandwich Islands where chinstrap penguins are most colonies is free of sea ice in December has increased in the abundant. It remains to be seen whether these southern last 20 years (Fig. 4). WAP chinstrap penguins differ from their more northern conspecifics with respect to breeding phenology, migration strategy, or foraging strategies. While chinstrap penguins Discussion are apparently able to successfully breed along the southern WAP, the biotic and abiotic constraints on greater expan- Despite a concerted search effort for new gentoo penguin sion of chinstrap colonization and persistence remain an colonies, we did not find any colonies south of Cape open question. We speculate that the rates of extinction for Tuxen. Our results coincide with the data collected by these small, isolated groups [as well as on other extremely Pilipenko (2013), which also confirmed the breeding pop- isolated islands such as Peter I Island, Heard Island, and the ulation at Cape Tuxen. All gentoo colonies for which it was Balleny Islands; see Woehler (1993)], would be high possible to estimate population change showed a signifi- absent at least occasional migration from more abundant cant increase in their breeding abundance, consistent with populations at the core of their breeding range, but the rates the general trend of gentoo penguin population growth of these processes are unknown. Given the lack of physi- along the WAP (Lynch et al. 2012). ological (or obvious ecological) barriers for breeding this Despite widespread population declines along most of far south, it is not clear why chinstraps are not more the WAP, we found that small numbers of chinstrap pen- abundant in this region. guins south of 65°S have persisted (Table 3). We report Relatively little is known about the abundance and here for the first time chinstrap penguins breeding in small distribution of blue-eyed shags in the area covered by this numbers as far south as Cone Island and Emperor Island, survey, and we have only sparse historical data for these the latter of which may now be the southern-most breeding populations to assess how the population might have population [given the apparent disappearance of the colony changed in the last few decades. At two of the more

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Table 4 Ade´lie penguin (Pygoscelis adeliae) colonies surveyed and references to data collected in previous years by other authors Map ID Locality Count Accuracy Year Reference

5 Port Charcot (Booth I.) 500 A5 1909 Croxall and Kirkwood (1979) 83 C1 1982 Poncet and Poncet (1987) 9 C1 2010 Pilipenko (2013) 15 N1 2012 This paper 7 Petermann I. 925 A3 1909 Croxall and Kirkwood (1979) 1,540 N3 1971 Mu¨ller-Schwarze and Mu¨ller-Schwarze (1975) 987 N1 1982 Airey (1982), in Poncet and Poncet (1987) 251 N1 2010 Pilipenko (2013) 283 N1 2012 This paper 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) 2,411 N1 2012 This paper 13 Berthelot Is. 904 N1 1982 Airey (1982), in Poncet and Poncet (1987) 346 N1 2010 Pilipenko (2013) 313 N1 2012 This paper 14 Rocks west of Trundle I. 347 N1 2012 This paper 15, 16, 17 and 18 Pitt Is. North (Jingle I., Weller I., 3,424 + 350 C1 + N3/4 1983 Poncet and Poncet (1987) Islet southeast of Weller I., and Smiggers I. combined) 1,059 N1 2012 This paper 19 Islet north east of Fitzkin I. 250 N3/4 1983 Poncet and Poncet (1987) 113 N1 2012 This paper 20 Two islets next to Winkle I. 52 C1 1982 Pitt Is. south in Poncet and Poncet (1987) 32 N1 2012 This paper 21 Vieugue I. 600 N4 1986 Poncet and Poncet (1987) 359 N1 2012 This paper 22 Islets south of Martin I. 1,277 C1 1982 “Kim Is.” in Poncet and Poncet (1987) 477 N1 2012 This paper 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) 912 N1 2012 This paper 26 Islet 1 km west of Lavosier I. 150 N4/5 1986 Poncet and Poncet (1987) 17 N1 2012 This paper 27 Cape Evensen (including 1,200 N3/4 1983 Poncet and Poncet (1987) penguins on offshore rocks) 1,100 N3/4 1990 Woehler (1993) 374 N1 2012 This paper 28 Darbel Islands 650 N3/4 1983 Poncet and Poncet (1987) 324 N1 2012 This paper 29 Kuno Point 235 N1 2012 This paper 30 Barcroft Is. 1,600 N4/5 1982 Poncet and Poncet (1987) 211 N1 2012 This paper 32 Holdfast Point 625 N3/4 1983 Poncet and Poncet (1987) 435 N1 2012 This paper

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Table 4 continued Map ID Locality Count Accuracy Year Reference

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) 1,104 C1 2012 This paper 35 Andresen I. (northeast coast) 281 N1 2012 This paper 36 Chatos I. 100 N4/5 1982 Poncet and Poncet (1987) 135 N1 2012 This paper 37 Cone I. 3,000 N4/5 1982 Poncet and Poncet (1987) 3,051 N1 2012 This paper 38 Bongrain Point (Pourquoi Pas I.) 700 N3/4 1983 Poncet and Poncet (1987) 2,284 N1 2012 This paper 39 Ginger I. 2,790 C1, C3 1982 Poncet and Poncet (1987) 3,334 C1 2012 This paper 40 Avian I. 25,000 A4 1968 Croxall and Kirkwood (1979) 35,600 N2 1978 Poncet and Poncet (1987) 77,515a N (unknown 2012 Sailley et al. (2013) precision) 47,146 C1 2012 This paper 41 Emperor I. 700 N4/5 1985 Poncet and Poncet (1987) 1,420 C1 2012 This paper 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) 7,482 C1 2012 This paper 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) 3,760 C1 2012 This paper 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 northern sites in our survey area (Pursuit Point and Rocks Primary productivity strongly correlated with trends west of Trundle Island), shag populations appear to be in Ade´lie abundance decreasing, while at two of the sites further south (Fish Islands and Ginger Island), they appear to be stable or even Persistent phytoplankton blooms in Marguerite Bay are increasing. This pattern is consistent with the general congruent with population numbers for Ade´lie populations north–south trend seen for Ade´lie penguins, though con- that are stable or increasing, suggesting a relationship tinued observation of blue-eyed shag populations will be between persistent primary productivity and maintenance required to understand their dynamics in the context of of Ade´lie populations. Referencing previous surveys in this underlying environmental conditions. Using the estimated region (Poncet and Poncet 1987; Woehler 1993) and the global population of 10,900 breeding pairs by Orta (1992) analyses reported in Lynch et al. (2012), it is clear that all as reported by Casaux and Barrera-Oro (2006), our survey Ade´lie populations from the Yalour Islands south to Mar- covered approximately 25 % of the global population of guerite Bay have declined, some by as much as 75 %. By Phalacrocorax (atriceps) bransfieldensis. contrast, the Ade´lie populations at eight open-ocean-facing

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Table 5 Blue-eyed shag (Phalacrocorax [atriceps] bransfieldensis) colonies surveyed Map ID Locality Count Accuracy Year Reference

1 Pursuit Point 140 Unknown 1986 Harris et al. (2011) 21 N1 2012 This paper 12 Green I. 89 N1 2012 This paper 14 Rocks west of Trundle I. 140 Unknown 1989 Harris et al. (2011) 71 N1 2012 This paper 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) 32 N1 2012 This paper 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) 78 N1 2012 This paper 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) 504 N1 2012 This paper 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 % sites in Marguerite Bay (Chatos Island, Cono Island, Gin- et al. 2013) and frequently hosts the largest and most ger Islands, Bongrain Point at Pourquois-Pas Island, Red persistent phytoplankton blooms on the WAP (Marrari Rock Ridge, Lagotellerie Island, Emperor Island, and et al. 2008). Spring and summer phytoplankton blooms are Avian Island) appear to be maintaining their size or an important factor influencing Antarctic krill (Euphausia increasing, consistent with other research suggesting that superba) recruitment in the Antarctic Peninsula region northern Marguerite Bay is a biological “hotspot” with (Marrari et al. 2008), which is widely recognized as a high occurrence rates of krill predators (Friedlaender et al. major link between primary producers and many popula- 2011). tions of krill-feeding vertebrates, including penguins The Marguerite Bay area is of particular interest because (Ballerini et al. 2014). It has been shown that there is an it has unique oceanographic characteristics (e.g., Schofield alongshore gradient of phytoplankton biomass in the

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Fig. 2 Ade´lie penguin population trends along with the A distribution of chlorophyll-a concentration (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-a concentration (2003–2014), b mean January chlorophyll-a N concentration for each year from 2003 to 2011. Note the persistence of the phytoplankton blooms in the Marguerite Bay area B

2003 2004 2005

2006 2007 2008

2009 2010 2011 Chlorophyll-a concentration Decreasing No change Increasing No data Low High northern part of the Antarctic Peninsula, with higher bio- shore regions, Marrari et al. 2008). However, the Mar- mass in the northern sectors earlier in the productive guerite Bay area showed persistently high chlorophyll season, which later progresses to the southeast as the sea concentrations (0.1–47 mg/m3) during spring and summer ice retreats (Smith et al. 1998; Garibotti et al. 2003). In this in comparison with any other sector west of the Antarctic area, intermediate values of chlorophyll-a were observed Peninsula (Marrari et al. 2008). Reports on chlorophyll-a (0.1–2 mg/m3) with small spatial extent, short-lived blooms concentrations in the Marguerite Bay area vary from (chlorophyll values greater than 2 mg/m3 in some near 2.30 mg/m3 (Arrigo and van Dijken 2003) to up to 17.86

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1998–2006 between Marguerite Bay and south of Anvers Island (63.8°–67.8°S, 64.4°–73.0°W)—an area where

3 data

50 100 150 Ade´lie penguin populations have been declining in the last

Frequency permuted

0 decades. We propose two possible explanations for this −0.2 0.0 0.2 0.4 Difference in group means 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

chlorophyll - a (mg/m ) the frequency of years with persistently high concentration

0.8 1.0 1.2 1.4 1.6 1.8 in the phytoplankton blooms over time may be more rel- evant to penguin population trends than an average trend No data Decreasing No change Increasing on phytoplankton concentration skewed by infrequent high Change in Adelie penguin colony abundance blooms (cf. Fraser and Hofmann 2003). It may also be the Fig. 3 Box plot showing January chlorophyll-a concentration (avail- case that this ecological boundary continues to move able from: http://oceancolor.gsfc.nasa.gov) around the colonies southward, so the line between increasing and decreasing grouped by the population status of the colonies. Boxes extend to the chlorophyll-a concentrations may have shifted further first and third quartiles and whiskers extend to the extrema (points [1.5 times the inter-quartile range from the box represented south since 2006 [the last year included in the analysis by by circles). Inset mean difference between the “increasing” and Montes-Hugo et al. (2009)]. “decreasing” group means under random permutation of the group = labels (n 999). Arrow indicates the empirical difference in group Summer sea ice declines improves colony access means, which is larger than any of the 999 random permutations (hence, p \ 0.001) In the last 30 years, summer sea ice extent has been declining in Marguerite Bay (Fig. 4). Our analysis of A summer sea ice in the proximities of penguin colonies p = 0.02 80 R2 = 0.14 showed that summer sea ice has declined at all sites, 40 especially since the late 1980s. The Marguerite Bay area 0 has essentially shifted from a regime of extensive summer B 1980 1985 1990 1995 2000 2005 2010 sea ice to less extensive summer sea ice, including years 80 p = 0.003 R2 = 0.23 with no summer sea ice (Fig. 4). Several studies have 40 highlighted that in breeding seasons with reduced summer 0 C 1980 1985 1990 1995 2000 2005 2010 sea ice adjacent to rookeries Ade´lie penguins are able to p < 0.001 use fat reserves and food for breeding purposes (egg pro- 80 R2 = 0.28 40 duction, courtship, incubation and chick feeding) instead of

Minimum sea−ice concentration (%) 0 using those resources for traveling to reach open water (at 1980 1985 1990 1995 2000 2005 2010 , Stonehouse 1963; at , Ainley and Year Leresche 1973; in the area, Taylor et al. 1990). Highlighting the potentially negative consequences of heavy summer sea ice, Croxall and Kirkwood (1979) noted Fig. 4 Minimum sea ice concentration for December around the that during the 1958–1959 breeding season in Detaille Marguerite Bay colonies. (Sea ice data available from the National Island, penguins had to walk nearly 50 km to reach open Snow and Ice Data Center: http://nsidc.org/). a Cone Island and Chatos Island; b Avian Island, Ginger Island and Emperor Island; and water, which led to almost complete nest failure in that c Bongrain Point (), Lagotellerie Island and Red year. Rock Ridge. The dotted line shows the general trend of sea ice con- Our survey data suggest that Ade´lie penguin populations centration for the sites flourish where persistently high primary productivity occurs in areas without extensive summer sea ice that and 25 mg/m3 (Garibotti et al. 2003; Meyer et al. 2003, might block access to the colony during the austral spring. respectively). In areas north of Marguerite Bay, loss of sea ice has It is interesting to compare our findings with Montes- increased access to the colony for breeding but at the Hugo et al. (2009), who find an unambiguous demarcation expense of reduced food availability for krill specialist between areas of decreasing chlorophyll-a (northern WAP) predators (Trivelpiece et al. 2011). We believe that Mar- and increasing chlorophyll-a (southern WAP). At the guerite Bay benefits from consistently high primary broadest scale, our findings are consistent with this picture. productivity, in part due to its unique hydrogeography However, Montes-Hugo et al. (2009) found that chloro- (Ashjian et al. 2004), and this mitigates regional losses of phyll-a has increased 66 % on average from 1978–1986 to krill habitat due to declining annual sea ice cover. At the 123 Polar Biol same time, decreasing sea ice is likely allowing Ade´lie Ainley D, Ballard G, Blight LK, Ackley S, Emslie SD, Lescroe¨lA, penguins to recoup any reduction in prey availability by Olmastroni S, Townsend SE, Tynan CT, Wilson P, Woehler E (2009) Impacts of cetaceans on the structure of reductions in net reproductive energy, with reduced for- food webs. Mar Mamm Sci 26:482–498 aging effort and greater efficiencies due to access to open Airey LR (1982) General report, 11 March 1982–28 February 1983. water. It is possible that continued reduction in sea ice will AD6/2F/1982/A. unpublished report exceed the threshold where the net benefit of access to the Arrigo KR, van Dijken GL (2003) Phytoplankton dynamics within 37 Antarctic coastal polynya systems. J Geophys Res 108:3271 colony is outweighed by concomitant loss of prey. Ashjian CJ, Rosenwaks GA, Wiebe PH, Davis CS, Gallager SM, While the biggest gains in Ade´lie penguin abundance in Copley NJ, Lawson GL, Alatalo P (2004) Distribution of the Marguerite Bay area have occurred between the mid- zooplankton on the continental shelf off Marguerite Bay, 1980s and the 2012/2013 season, it is interesting to note Antarctic Peninsula, during austral fall and winter, 2001. Deep Sea Res II 51:2073–2098 that these populations have been increasing at least since Ballerini T, Hofmann EE, Ainley DG, Daly K, Marrari M, Ribic CA, the 1940s. For example, Croxall and Kirkwood (1979) Smith WO, Steele JH (2014) Productivity and linkages of the noted that “a real increase in numbers [at Lagotellerie food web of the southern region of the western Antarctic Island] had taken place by the late 1940s–early 1950s”. Peninsula continental shelf. Prog Oceanogr 122:10–29 Casaux R, Barrera-Oro E (2006) Shags in Antarctica: their feeding Therefore, while recent gains in abundance may be behaviour and ecological role in the marine food web. Antarct explained by improving sea ice conditions (from the per- Sci 18:3–14 spective of access to breeding colonies), increases earlier in Clarke A, Murphy EJ, Meredith MP, King JC, Peck LS, Barnes DKA, the twentieth century prior to increasing air temperatures Smith RC (2007) Climate change and the marine ecosystem of the western Antarctic Peninsula. Philos Trans R Soc Lond Ser B and declining sea ice (King and Turner 1997; Smith and 362:149–166 Stammerjohn 2001) are not easily explained by abiotic Croxall JP, Kirkwood ED (1979) The distribution of penguins on the drivers. These increases may reflect a response to har- Antarctic Peninsula and islands of the Scotia Sea. British vesting of other krill predators (e.g., seals and whales), as Antarctic Survey, Cambridge, UK Croxall JP, Trathan PN, Murphy EJ (2002) Environmental change and reviewed by Ainley et al. (2009), though the data on pen- Antarctic seabird populations. Science 297:1510–1514 guin abundance we have for this region are insufficient to Ducklow HW, Fraser WR, Meredith MP, Stammerjohn SE, Doney make any firm conclusions in this regard. SC, Martinson DG, Sailley SF, Schofield OM, Steinberg DK, While logistical difficulties in accessing the southern Venables HJ, Amsler CD (2013) West Antarctic Peninsula: an ice-dependent coastal marine ecosystem in transition. Oceanog- portion of the WAP make it difficult to census these pop- raphy 26:190–203 ulations regularly, it is clear that Marguerite Bay and areas Fraser WR, Hofmann EE (2003) A predator’s perspective on causal just north are not just static “predator hotspots” but rep- links between climate change, physical forcing and ecosystem resent the leading edge of climatic changes that can bring response. Mar Ecol Prog Ser 265:1–15 Fraser WR, Trivelpiece WZ, Ainley DG, Trivelpiece SG (1992) transient benefits to species such as penguins. Whether Increases in Antarctic penguin populations: reduced competition Marguerite Bay will remain a refugium for Ade´lie pen- with whales or a loss of sea ice due to environmental warming? guins on the WAP in the long term remains to be seen, but Polar Biol 11:525–531 clearly this is a region deserving of focused attention over Friedlaender AS, Johnston DW, Fraser WR, Burns J, Halpin PN, Costa DP (2011) Ecological niche modeling of sympatric krill the next several decades. predators around Marguerite Bay, Western Antarctic Peninsula. Deep Sea Res II 58:1729–1740 Acknowledgments We gratefully acknowledge the support of The Gain L (1914) Oiseaux antarctiques. Deuxie`me Expe´dition Antarc- Tinker Foundation, whose support enabled Oceanites, Inc. and the tique Franc¸aise 1908–1910 Antarctic Site Inventory team to charter Golden Fleece for this Garibotti IA, Vernet M, Ferrario ME, Smith RC, Ross RM, Quetin LB directed research, and in addition, thank the U.S. National Science (2003) Phytoplankton spatial distribution patterns along the Foundation Office of Polar Programs and Geography and Spatial western Antarctic Peninsula (Southern Ocean). Mar Ecol Prog Sciences (Awards Nos. 07-39515 and 12-55058). We also acknowl- Ser 261:21–39 edge the support of NASA headquarters under the NASA Earth and Harris CM (ed) (2006) Wildlife awareness manual: Antarctic Space Fellowship Program—Grant NNX10AN55H to P. C. We are Peninsula, , . grateful to the crew of the yacht Golden Fleece, Yoann Gourdet and Wildlife Publication No. 1. Prepared for the UK foreign and Cathy Colle, for ensuring the safety and well-being of the Antarctic commonwealth office and HMS endurance. Environmental Site Inventory research team during their work period in the Antarctic Research and Assessment, Cambridge Peninsula. Cheesemans’ Ecology Safaris and One Ocean Expeditions, Harris CM, Carr R, Lorenz K, Jones S (2011) Important bird areas in which graciously provided transportation to and from the Peninsula. Antarctica: Antarctic Peninsula, South Shetland Islands, South Orkney Islands—final report. Prepared for Birdlife International and the Polar Regions Unit of the UK foreign and common- wealth office. Environmental Research and Assessment Ltd., Cambridge References King JC, Turner J (1997) Antarctic meteorology and climatology. Cambridge University Press, Cambridge Ainley DG, Leresche RE (1973) The effects of weather and ice Lynch HJ, LaRue MA (2014) First global survey of Ade´lie penguin conditions on breeding in Ade´lie Penguins. Condor 75:235–239 populations. Auk 131:457–466

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Lynch HJ, Naveen R, Fagan WF (2008) Censuses of penguins, blue- Pilipenko DV (2013) Colonial bird species breeding in the UAS, Akademik eyed shags, and populations in the Antarctic Vernadsky 2010–2011 season. УКPAЇHCЬКИЙ AHTAPКTИЧHИЙ Peninsula. Mar Ornithol 36:83–97 ЖУPHAЛУAЖ (Ukr Antarct J UAZH) 12:206–216 Lynch HJ, Naveen R, Trathan PN, Fagan WF (2012) Spatially Poncet S, Poncet J (1987) Censuses of penguin populations of the integrated assessment reveals widespread changes in penguin Antarctic Peninsula, 1983–87. Br Antarct Surv Bull 77:109–129 populations on the Antarctic Peninsula. Ecology 93:1367–1377 Sailley SF, Ducklow HW, Moeller HV, Fraser WR, Schofield OM, Lynch HJ, Naveen R, Casanovas PV (2013) Antarctic site inventory Steinberg DK, Garzio LM, Doney SC (2013) Carbon fluxes and breeding bird survey data 1994/95–2012/13. Ecology 94:2653 pelagic ecosystem dynamics near two western Antarctic Penin- Marrari M, Daly KL, Hu C (2008) Spatial and temporal variability of sula Ade´lie penguin colonies: an inverse model approach. Mar SeaWiFS chlorophyll a distributions west of the Antarctic Ecol Prog Ser 492:253–272 Peninsula: implications for krill production. Deep Sea Res II Schofield O, Ducklow H, Bernard K, Doney S, Patterson-Fraser D, 55:377–392 Gorman K, Martinson D, Meredith M, Saba G, Stammerjohn S, Meyer B, Atkinson A, Blume B, Bathmann U (2003) Feeding and Steinberg D, Fraser W (2013) Penguin biogeography along the energy budgets of larval Antarctic krill, Euphausia superba,in West Antarctic Peninsula. Oceanography 26:204–206 summer. Mar Ecol Prog Ser 257:167–177 Smith RC, Stammerjohn SE (2001) Variations of surface air Montes-Hugo M, Doney SC, Ducklow HW, Fraser W, Martinson D, temperature and sea-ice extent in the western Antarctic Penin- Stammerjohn SE, Schofield O (2009) Recent changes in sula region. Ann Glaciol 33:493–500 phytoplankton communities associated with rapid regional Smith RC, Baker KS, Vernet M (1998) Seasonal and interannual climate change along the western Antarctic Peninsula. Science variability of phytoplankton biomass west of the Antarctic 323:1470–1473 Peninsula. J Mar Syst 17:229–243 Mu¨ller-Schwarze C, Mu¨ller-Schwarze D (1975) A survey of twenty- Smith RC, Ainley D, Baker K, Domack E, Emslie S, Fraser B, four rookeries of pygoscelid penguins in the Antarctic Peninsula Kennett J, Leventer A, Mosley-Thompson E, Stammerjohn S region. In: Stonehouse B (ed) The biology of penguins. (1999) Marine ecosystem sensitivity to climate change. Biosci- University Park Press, Baltimore, pp 309–320 ence 49:393–404 Murphy EJ, Watkins JL, Trathan PN, Reid K, Meredith MP, Thorpe Taylor RH, Wilson RP, Thomas BW (1990) Status and trends of SE, Johnston NM, Clarke A, Tarling GA, Collins MA, Forcada J, Ade´lie penguin populations in the Ross Sea region. Polar Record Shreeve RS, Atkinson A, Korb R, Whitehouse MJ, Ward P, 26:293–304 Rodhouse PG, Enderlein P, Hirst AJ, Martin AR, Hill SL, Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecological Staniland IJ, Pond DW, Briggs DR, Cunningham NJ, Fleming segregation of Ade´lie, gentoo, and chinstrap penguins at King AH (2007) Spatial and temporal operation of the Scotia Sea George Island, Antarctica. Ecology 68:351–361 ecosystem: a review of large-scale links in a krill centred food Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, web. Philos Trans R Soc Lond Ser B 362:113–148 Watters GM (2011) Variability in krill biomass links harvesting Naveen R, Lynch HJ (2011) Antarctic Peninsula compendium, 3rd and climate warming to penguin population changes in Antarc- edn. Environmental Protection Agency, Washington, DC tica. Proc Natl Acad Sci USA 108:7625–7628 Orta J (1992) Family Phalacrocoracidae (Cormorants). In: del Hoyo J, Woehler EJ (1993) The distribution and abundance of Antarctic and Elliot A, Sargatal J (eds) Handbook of the birds of the world, vol sub-Antarctic penguins. Scientific Committee on Antarctic 1. Lynx editions, Barcelona, pp 326–353 Research, Cambridge

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