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Emperor Penguins Breeding on Iceshelves

Emperor Penguins Breeding on Iceshelves We describe a new breeding behaviour discovered in emperor penguins; utilizing satellite and aerial-survey observations four emperor penguin breeding colonies have been recorded as existing on ice-shelves. Emperors have previously been considered as a sea-ice obligate species, with 44 of the 46 colonies located on sea-ice (the other two small colonies are on land). Of the colonies found on ice-shelves, two are newly discovered, and these have been recorded on shelves every season that they have been observed, the other two have been recorded both on ice-shelves and sea-ice in different breeding seasons. We conduct two analyses; the first using synthetic aperture radar data to assess why the largest of the four colonies, for which we have most data, locates sometimes on the shelf and sometimes on the sea-ice, and find that in years where the sea-ice forms late, the colony relocates onto the ice-shelf. The second analysis uses a number of environmental variables to test the habitat marginality of all emperor penguin breeding sites. We find that three of the four colonies reported in this study are in the most northerly, warmest conditions where sea-ice is often sub-optimal. The emperor penguin’s reliance on sea-ice as a breeding platform coupled with recent concerns over changed sea-ice patterns consequent on regional warming, has led to their designation as ‘‘near threatened’’ in the IUCN red list. Current climate models predict that future loss of sea-ice around the Antarctic coastline will negatively impact emperor numbers; recent estimates suggest a halving of the population by 2052. The discovery of this new breeding behaviour at marginal sites could mitigate some of the consequences of sea-ice loss; potential benefits and whether these are permanent or temporary need to be considered and understood before further attempts are made to predict the population trajectory of this iconic species. Citation: Fretwell PT, Trathan PN, Wienecke B, Kooyman GL (2014) Emperor Penguins Breeding on Iceshelves. PLoS ONE 9(1): e85285. doi:10.1371/ journal.pone.0085285 Editor: Antoni Margalida, University of Lleida, Spain Received June 27, 2013; Accepted December 4, 2013; Published January 8, 2014 Copyright:  2014 Fretwell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding for this study came internally from BAS-NERC ecosystems programme. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No current external funding sources for this study. Competing Interests: The authors have declared that no competing interests exist. * E-mail: ptf@bas.ac.uk obligate, the species is too clumsy to climb onto ice shelves and Introduction needs ice of a low freeboard to exit the ocean [2]. Of the 46 Recent studies suggest that emperor penguin populations will colonies presently known 44 breed on fast-sea- ice [13] (stable sea- decline in future decades due to climate change [1–6]. Current ice attached to the coast). Of the two remaining colonies, one is projections suggest that the world population will halve before recorded as breeding on rock and one on a frozen lake, both of 2052[3] with more northerly colonies, above 70uS being lost these colonies are small, one having a recorded population of 2900 entirely [6]. This has led the IUCN to re-list the species from pairs and the other 250 pairs [13] (the mean colony size is ‘‘Least Threatened’’ to ‘‘Near Concern’’ [7]. The primary reason approximately 5500 pairs). cited for this predicted decline is the species’ reliance on sea-ice, a In recent years satellite observations have improved our habitat that is expected to decrease in future years [8,9]. Sea ice is knowledge of the emperor penguins breeding distribution [14] important to the species in two ways; firstly as a breeding platform and population [13]. Here we report on newly discovered and secondly as a foraging environment. A decrease in sea-ice breeding behaviour in emperor penguins seen from satellite and distribution will negatively impact food webs [10], reducing aerial surveys. Four emperor colonies have been observed numbers of Krill (Euphausia superb), and the higher trophic levels which breeding on ice-shelves not sea-ice The first, discovered in feed on Krill such as glacial squid (Pleuragramma antarcticum); two species 2009[15]on the West Ice Shelf at the edge of Barrier Bay was a which compose the majority of the emperors diet [11]. A decrease small colony of that could have been judged an anomaly or a in food availability may negatively affect survival, breeding break off group from the larger West Ice shelf colony located success, recruitment and therefore population size. ,110 km to the north. However, since the discovery of the As a breeding platform, stable or ‘‘fast’’ sea-ice is required which colonies on the West Ice Shelf, three other, large colonies, have forms when the emperors arrive at their breeding locations (usually been found that are either permanently, or annually located on ice in April) and remains unbroken until the chick fledge (usually in shelves rather than on sea-ice. December). If the sea-ice breaks up too early in the season it will Whereas sea-ice is frozen sea-water, ice-shelves are floating result in high chick mortality [1–6], multiple years of poor sea-ice glacial ice that has flowed from the land into the sea; where the will lead to poor breeding success, population decline and eventual base of such glaciers breaks hydrostatic equilibrium, the ice-foot extinction of a colony [12]. The emperor penguin is a sea-ice detaches from the ground bed and the glacial ice floats. When a PLOS ONE | www.plosone.org 1 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves single glacier feeds into the sea a glacier tongue is formed, but group was located near the edge of the ice cliff of the West Ice around the Antarctic coastline it is more common for ice from Shelf. The birds had accessed the ice shelf via an ice gully several glaciers or ice-streams to merge to form an ice-shelf. At approximately 5km to the southeast. The colony has been their terminus ice-shelves can form ice cliffs, in some place over 60 observed in three subsequent years in the same position. The metres high, although a few tens of metres is more common. Ice presence of chicks at Barrier Bay confirms that this is a breeding creeks often indent the cliff face giving a potential route up onto location rather than a temporary site (Figure 1). the ice-shelf itself, or where ice shelves are ablating the ice cliff may The second colony identified on the top of an ice shelf is the be less steep. As sea-ice forms, local weather conditions mean it Shackleton Ice Shelf colony. This colony was first located in 2008 can be highly variable in extent and duration, and therefore highly [14] at 64.86uS, 96.02uE. The December 2008 position, found by susceptible to regional climate change [8]. Ice-shelves are less Landsat imagery and later confirmed by Very High Resolution dynamic, and are less susceptible to weather patterns and storm (VHR) satellite imagery (November 2009), was on sea-ice. The events, although cyclical calving events could pose a threat to colony comprised approximately 6,470 pairs [13]; satellite organisms located near the ice-cliff edge and over longer time observations confirmed that the breeding location remained periods ice-shelves can collapse catastrophically such as the well constant in 2008, 2009 and 2010. However, in 2011 it appeared documented break-up of the Larsen B Ice Shelf in 2002[16]. 15km to the south (64.98uS, 96.06uE) of its original location and It is at present unclear whether this behaviour of breeding on ice on top of the ice shelf. The access route to the top of the shelf was a shelves is a new phenomenon associated with recent climate gulley 3.4 km to the east. In 2012, the breeding location was the same as in 2011 (Figure 2). change, or one that has always existed but has not yet been documented. Models of how animals adapt to climatic change The third breeding location on top of an ice shelf is near the exist [17] and we examine how this phenotype plasticity fits into Jason Peninsula, at the northern limit of the Larsen C Ice Shelf. In those theories (see discussion). 1893, the explorer and sealer Carl Anton Larsen was the first to That emperor penguins can move their breeding site depending visit this area [18,19]. He reported on 4 December 1893 that ‘‘The upon ice conditions to a more stable location, including onto the kongepenguinerne (king penguin) are very numerous in those (ice) top of the ice-shelf itself, means new factors should be incorporated fjords’’ (ice creeks are a favoured breeding location of emperor into modelled population trajectories for this species. Whether penguin colonies). When recording this, his ship was located on such factors will provide temporary or permanent relief from the the northern side of what became known as the Larsen C Ice Shelf (noon position of 67.00uS, 60u.00W). At the time of this discovery impacts of climate change remains uncertain. The fact that emperors exhibit a previously unknown breeding little was known about emperor penguins and they were often behaviour, intimates that other less-well known species may also confused with the similar, but smaller king penguin (A. patagonicus), a species which Larsen would have been familiar with from his have similar unknown adaptive behaviours that may also offer temporary or permanent relief to the challenges of climate change. sealing trips to South Georgia. It is likely that Larsen’s sighting late in the breeding season indicated a colony in the vicinity. Although exhaustive satellite searches of the sea-ice in the area during Materials and Methods previous studies [14,15] were conducted, no colony was found. Observations However, in 2012, a further satellite survey for emperor colonies The first emperor colony found on an ice shelf was the Barrier was conducted along the edge of the Larsen C Ice Shelf. A Bay colony, 67.22uS, 81.93uE discovered in December 2009 [14]. medium sized colony was discovered on top of the shelf (at Some 295 chicks and a small number of adults were seen. The 66.08uS, 60.65uW). An aerial survey of the colony was undertaken Figure 1. Envisat images showing the sea-ice conditions in late March around the West Ice shelf where two emperor colonies are located (equivalent imagery for 2009 is not available). Darker areas denote poor sea-ice, grey shows thicker sea-ice and white indicates ice shelf. Note that the Barrier Bay colony has a permanent polynya while the West Ice shelf colony located on the sea-ice has thicker sea-ice at this time of year when the birds would be arriving in the area to breed (images courtesy of Polarview – www.polarview.aq). doi:10.1371/journal.pone.0085285.g001 PLOS ONE | www.plosone.org 2 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Figure 2. Shackleton Ice Shelf very high resolution satellite image. WorldView2 image (15 September 2012) showing the location of the Shackleton Ice shelf colony in 2012 in context with the ice edge. On this image the four main sub-colonies are clearly visible on top of the Shackleton PLOS ONE | www.plosone.org 3 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Ice Shelf around 5 km from the ice cliffs that form the edge of the ice shelf. The image data also clearly shows groups of penguins on their way to and from the ice edge, and the tracks they leave behind them. By marking these trails it is possible to assess where each group has come from and which direction it is heading. Interestingly at this site, the outgoing forages use a different route to the incoming penguins; on the way out they negotiate a large ice cliff. ICESAT data from the area suggest that the top of the ice sheet is 32–34 m high, the image shows no slope down to the cliff so the drop may be considerable (although there is evidence of large snowdrifts abutting the cliff). The incoming parties cannot negotiate the cliff and so take a 5 km longer route around the edge of the ice shelf until they can access the gentle slopes afforded by a number of ice creeks to the east of the colony. How the emperor penguins get down the ice cliff is, at present, unclear. doi:10.1371/journal.pone.0085285.g002 in early December 2012 (Figure 3) revealing that the colony above the ice cliff (Figure 5). At present no information is available comprised around 3,800 adult birds. Archival satellite imagery to suggest why the colony moved onto the shelf in this year. shows that it has been located on the ice shelf since at least 2008, the earliest imagery available for the area. The Antarctic Peninsula Analyses is one of the fastest warming regions [20] and has suffered To assess why the colony location had moved from sea-ice to significant ice shelf loss [21]. The sea-ice regime here has also been ice-shelf ENVISAT synthetic aperture radar imagery of sea-ice affected by climatic forcing and the birds may have moved from concentration was acquired of the Shackleton Ice shelf colony (for the sea-ice creeks to the top of the ice shelf. Exactly how the birds which the most data existed) several times over the course of the access the shelf is unclear but it appears that they climb the low ice breeding season. The imagery from March, when adults start to cliff (Figure 4). King penguins climb up dry glaciers in warm return to their breeding location [22], shows that in 2008, 2009 weather to stay cool; perhaps the less agile emperor is also able to and 2010 the sea-ice concentration at the initial site was dense and climb slopes, particularly where ice shelves weather and ablate the was sufficiently stable for the penguins to access the location steepness of the shelf face. (Figure 6). But in 2011 and 2012, the sea-ice did not form until Finally, a colony was sighted on top of an ice shelf at the early- to mid-April. The birds therefore chose a site on top of the Ruppert Coast colony. This colony was only discovered in 2010 ice shelf in years when sea-ice formed late. The birds show when it was located on the sea-ice under the ice cliffs of the remarkable fidelity to the site, changing their breeding platform in Nickerson Ice Shelf at 75.38uS, 143.35uW. Satellite imagery shows preference to changing the breeding location when April sea-ice that in 2008, 2011 and 2010 (no images from 2009 are available) conditions become unsuitable. the colony was located on the sea-ice at 75.38uS, 143.28uW, but in To test whether the presence of colonies that have been found 2012 (17/10/2012) it had moved onto the edge of the ice shelf on ice-shelves was linked to environmental conditions, three Figure 3. Emperor penguins on the edge of the Larsen Ice Shelf near the Jason Peninsula late in the breeding season. The larger group is on the ice-shelf, the smaller group has moved onto the fast-ice; earlier in the season data from QuickBird1 satellite imagery shows that the whole colony was located on the ice-shelf. Note the ice cliff which is probably an insurmountable barrier to the adult emperor penguins. No evident route to the colony was determined from the images. (Photo Ian Potten). doi:10.1371/journal.pone.0085285.g003 PLOS ONE | www.plosone.org 4 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves PLOS ONE | www.plosone.org 5 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Figure 4. A and B; maps showing location of the Jason Peninsula colony. C: Quickbird1 image (12 Sept 2012) showing the main Jason Peninsula emperor penguin colony in relation to the ice-shelf and sea ice edge. D: Emperor penguins (small black dots) on their way to or from the breeding colony onto of the sea-ice. They have to climb up or down a small ice cliff, which shows up as white in this image. To the left of this cliff is ice shelf, while the ridged area to the right is fast-ice. In this image emperors can be seen on the ice shelf (a long line in upper left and parallel to the cliff face) and the cliff (shorter linear group at middle bottom and perpendicular to the cliff face). The height of this ice cliff is presently unknown but based on the size of the penguins in the image it may be only a few metres high. doi:10.1371/journal.pone.0085285.g004 environmental variables were assessed at the four sites and catalogue number 101001000A9A8B00 November 12th 2009 ), compared with values for other emperor penguin colony locations a possible response to poor sea-ice earlier in the season. A similar (Figure 7). Autumn (March/April) sea-ice concentration was behaviour has been observed at the Mertz Glacier colony which is also located in an area that has a high mean temperature (Andre´ modelled using synthetic aperture radio imagery from the Polarview website (http://www.polarview.aq/), mean temperature Ancel pers coms.). This behaviour at these other colonies suggests that breeding on ice-shelves is only one of several possible was assessed using the RACMO region climate model [23] and adaptations that could be employed by emperor penguins when latitude using the recent calculation of the circumpolar emperor sea-ice conditions are poor; others include moving onto land (for penguin population [13]. example Dion Islands). Of the other warmer sites the Snow Hill Island colony has not only the warmest mean temperature but is Results and Discussion also is the highest latitude, although it has a reasonable high mean Of the four colonies described here, the three that have been sea-ice concentration. Bowman Island has the third highest mean found breeding on ice shelves in multiple years could be described temperature and the fourth lowest sea-ice concentration. These as located in marginal conditions. The Shackleton Ice Shelf and two must be considered some of the most marginal and potentially Barrier Bay sites have the lowest mean autumn sea-ice concen- vulnerable of emperor breeding locations as neither colony has the trations of any colonies and both these and the Larsen ice-shelf option of moving onto floating ice-shelves as there are none in the colony are in the most northerly part of the emperors range and nearby locality and neither has it shown evidence of breeding on have higher-than-average mean-temperature regimes. Three other icebergs. colonies have mean annual temperatures higher than the Larsen The Ruppert Coast colony that has been found located on the colony; Smyley Island, Bowman Island and Snow Hill Island. On edge of an ice shelf in one year is neither in a warm or poor sea-ice Smyley Island in 2009 the colony was observed by QuickBird location; as yet we have no explanation of why this colony moved satellite imagery breeding on top of an iceberg (QuickBird to a more elevated location. Figure 5. QuickBird 2 very high resolution satellite image of the Ruppert Coast emperor penguin colony(17 October 2012) including part of the Ruppert Coast and Nickerson Ice Shelf, it clearly shows the emperor penguin colony located on the higher ice shelf. Access to the main colony seems to be by a shallow ice ramp north and west of the present location. Brown guano stains mark the previous colony site approximately half a kilometres northeast, and to the west, on the sea-ice is a smaller subgroup of penguins. doi:10.1371/journal.pone.0085285.g005 PLOS ONE | www.plosone.org 6 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves th Figure 6. Sea-ice concentration around the Shackleton Ice Shelf for the time period 2007 to 2012, each from the 20 of March. White shading denotes thick sea-ice; blue, thinner sea-ice; black, open water. The red dot shows the location of the breeding colony identified from QuickBird VHR imagery (images courtesy of Polarview/University of Bremen). doi:10.1371/journal.pone.0085285.g006 Only a relatively small number of emperor colonies have been shelves, as reported here, has only been reported once at a small studied across Antarctica [1,12,22,24], with the longest study colony in East Antarctica [15]. That this behaviour is not the based at Pointe Ge´ologie, which has been continually monitored exception but is apparently more common among emperor since the 1950s [1,4,5,24]. The behaviour of breeding on ice- penguins is a surprising result. The reasons why this behaviour Figure 7. Marginality. Histogram of three parameters at emperor penguin breeding colonies: blue bars represent mean March/April sea-ice concentration, red bars are latitude and green are mean temperature. Colonies are ranked from left to right with lowest sea-ice concentrations to the left. The four colonies mentioned in this paper are named in bold. Dashed lines in blue, red and green denote the mean of the three parameters for all colonies. Shackleton Ice shelf and Barrier Bay colonies are in locations that have the lowest mean autumn sea-ice concentrations. The Larsen ice shelf colony has slightly lower than average sea-ice concentrations, but its latitude and mean annual temperature are well above average. The colony on the far left, Dion Islands, marked in red is believed to have declined and ceased to exist following recent climate change (temperature rise and sea- ice loss) on the Antarctic Peninsula. This previously occupied site is included to give an indication of the current breeding limits. These parameters give no indication of why the Ruppert Coast colony, found breeding on the ice shelf in only one year, relocated onto this ice shelf in 2012. Mean sea- ice concentration (blue) is recorded as a percentage for March/April when emperors prospect and recruit at breeding sites. The figures are calculated using synthetic aperture radar measurements for all dates in these two months for the years 1998–2007. Latitude (red) is the latitude of the colony location from Fretwell et al. 2012 and Wieneke 2012, with the addition of the newly found Larsen Ice Shelf colony described in this paper. Mean temperature is based on a yearly mean for 2000–2004 based on the RACMO climate model. doi:10.1371/journal.pone.0085285.g007 PLOS ONE | www.plosone.org 7 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves has not been recorded before are unclear, possible explanations For emperor penguins, the loss of the sea-ice as a breeding include: platform is not the only consequence of a warming environment. Factors, such as changes to food webs [10,29] and increased 1. The phenomenon may be recent phenotypic plasticity as predation and competition [12] will also affect breeding success regional climate change affects parts of the Antarctic coastline. survival rates and other demographic parameters in areas that 2. Most previous study-sites are not located at ice-shelf breeding experience regional warming. Additionally, there are several colonies where this behaviour is exhibited. negative factors that could potentially result from breeding on 3. There have been no large scale systematic searches for ice shelves, including the lack of shelter and exposure to katabatic emperors on ice shelves (although many flights and surveys winds, lack of fresh snow in areas where increased wind speeds have overflown iceshelves). scour the surface and a risk from calving ice fronts. How great these risks are and how much of an advantage or disadvantage Visser [17] has proposed a number of possible adaptations to breeding on ice-shelves proves to be for this species has yet to be climate change in birds, including phenotype plasticity, which quantified. This new discovery also leads to a number of other includes changes in breeding behaviour. One special case of potential behavioural questions. For example: How do emperors phenotype plasticity noted in the work is that of ‘‘learning’’ where access the ice shelves? Does the breeding cycle differ in locations animals can adapt to climate change if they learn from their such as at the Larsen colony where breeding on ice-shelves has experiences. Whether the adaptation of emperor penguins become the norm? What is the energetic cost of scaling the ice- breeding on ice-shelves is learnt, or inherited behaviour is at front? Such questions will be important future topics of research. present unclear; the Larsen and Barrier Bay colonies seem to be Currently, sea-ice conditions and their predicted decline are one permanently located on the shelf, but the Shackleton colony moves of the key inputs into models that suggest large decreases in there only when sea-ice conditions in April dictate. One aspect of emperor penguin numbers. Therefore, the suitability of ice-shelves Visser’s work that must be considered is that it concentrates on versus sea-ice as a breeding platform for emperors urgently needs individual nesting birds rather than colonial species. Colonial quantifying. Future research efforts need to assess which colonies species, especially emperor penguins, seem to move en-mass to could potentially move to ice-shelves and whether this newly new locations, although how this decision is made is unclear. The described behaviour is a temporary or partial solution for coping previous work may not therefore prove an ideal model for with future climate change. Emperors are often portrayed as a assessing how colonial nesting sea-birds may adapt to climate barometer for the ecosystem, that is, a ‘‘canary in the coalmine’’ change. for species more difficult to study. This previously unknown and The ability of emperor penguins to change their breeding surprising behaviour recorded in such an iconic animal suggests platform when fast ice conditions deteriorate may be an important that other species may also be capable of unpredicted or unknown adaptation that could help the species survive in a warming behavioural adaptations that may also increase their survival in a environment. Although regional warming has led to loss of ice- future warming world. shelves around the Antarctic Peninsula [21] ice-shelves are less sensitive to a warming environment and react to warming on Author Contributions slower timescales than sea-ice, the extent, stability and seasonality of which can change rapidly with warming temperatures as Conceived and designed the experiments: PTF PNT BW GLK. Performed already seen in the Arctic [25,26,27,28] and in the west Antarctic the experiments: PTF. Analyzed the data: PTF BW. Contributed reagents/ Peninsula [8]. materials/analysis tools: PTF. Wrote the paper: PTF PNT BW GLK. References 1. Barbraud C, Weimerskirch H (2001) Emperor penguins and climate change. 12. Trathan PN, Fretwell PT, Stonehouse B (2011) First Recorded Loss of an Nature 411, 183–186. Emperor Penguin Colony in the Recent Period of Antarctic Regional Warming: 2. Ainley DG, Clarke ED, Arrigo K, Fraser WR, Kato A, et al. (2005) Decadalscale Implications for Other Colonies PLoS ONE 6; e14738: doi:101371/journal- changes in the climate and biota of the Pacific sector of the Southern Ocean, pone0014738. 1950s to the 1990s. Ant Sci 17; 171–182. 13. Fretwell P T, LaRue MA, Morin Pl, Kooyman GL, Wienecke B, et al. (2012) An 3. Ainley D, Russell J, Jenouvrier S, Woehler E, Lyver P, et al. (2010) Antarctic Emperor Penguin population estimate: The first global, synoptic survey of a penguin response to habitat change as Earth’s troposphere reaches 2uC above species from space. Plos One, 7 (4). 11,pp.0.1371/journal.pone.0033751. preindustrial levels Ecol Monogr 80; 49–66. 14. Fretwell PT, Trathan PN (2009) Penguins from space: faecal stains reveal the 4. Jenouvrier S, Barbraud C, Weimerskirch H (2005) Long term contrasted location of emperor penguin colonies. Glob. Ecol. Biogeogr. 18, 543–552. responses to climate of two Antarctic Seabird species. Ecology 86; 2889–2903. 15. Wienecke B (2012) Emperor penguins at the West Ice Shelf. Polar Biol. 35, 5. Jenouvrier S, Caswell H, Barbraud C, Holland M, Stroeve J, et al. (2009) 1289–1296. Demographic models and IPCC climate projections predict the decline of an 16. Rack W, Rott H (2004) Pattern of retreat and disintegration of the Larsen B ice emperor penguin population. Proceedings on Natl Acad Sci U S A 106; 1844– shelf, Antarctic Peninsula. Annals of Glaciology, 39 505–510. 17. Visser ME (2008) Keeping up with a warming world: assessing the rate of 6. Massom RA, Stammerjohn SE (2010) Antarctic sea ice change and variability – adaptation to climate change. PRSB 275, 649–659. Physical and ecological implications Polar Science 4; 149–186.IUCN. IUCN 18. Wienecke B (2010) The history of the discovery of emperor penguin colonies, Red list of threatened species. Version 2012–2. Available: www.iucnredlist.org. 1902–2004 Polar Rec. 46, 271–276. Downloaded on 5 May 2013. 19. Larsen CA (1894) The voyage of the ‘‘Jason’’ to Antarctic regions. Geogr. J. 7. IUCN. IUCN Red list of threatened species. Version 2012–2. Available: www. 4,333–344. iucnredlist.org. Downloaded on 5 May 2013. 20. Morris EM, Vaughan DG (2003) in Antarctic Peninsula Climate Variability: Historical 8. Stammerjohn SE, Martinson DG, Smith RC, Yuan X, Rind D (2008) Trends in and Paleoenvironmental Perspectives, (ed. Domack, E. et al. Antarct. Res. Ser., 79 61– Antarctic annual sea ice retreat and advance and their relation to El Nin,o– 68 (AGU, Washington, D. C., doi:10.1029/AR079p0061. 2003). Southern Oscillation and Southern Annular Mode variability. J Geophys Res 21. Cook AJ, Vaughan DG (2010) Overview of areal changes of the ice shelves on 113, C03S90: doi:101029/2007JC004269. the Antarctic Peninsula over the past 50 years. The Cryosphere 4, 77–98 9. Turner J, Bindschadler RA, Convey P, Di Prisco G (2009) Antarctic Climate doi:10.5194/tc-4-77-2010. Change and the Environment. Cambridge; SCAR UK 526p. 22. Kooyman G (1993) Breeding habitats of emperor penguins in the western Ross 10. Forcada J, Trathan PN (2009) Penguin responses to climate change in the Sea. Antarct. Sci. 5, 743–148. Southern Ocean Glob Change Biol 15: 1618–1630. doi: 101111/j1365- 23. Van Lipzig NP, Van Meijgaard E, Oerlemans J (2002) The spatial and temporal 2486200901909x. variability of the surface mass balance in Antarctica: results from a regional 11. Klages N (1989) Food and Feeding Ecology of Emperor Penguins in the Eastern atmospheric climate model. Int J. Climatol. 22, 1197–1217. Weddell Sea. Polar Biol. 9, 385–390. PLOS ONE | www.plosone.org 8 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves 24. Barbraud C, Gavrilo M, Mizin Y, Weimerskirch H (2011) Comparison of 27. Sime LC, Wolff EW, Oliver KIC, Tindall JC (2009) Evidence for warmer emperor penguin declines between Pointe Ge´ologie and Haswell Island over the interglacials in East Antarctic ice cores. Nature 462, 342–345. past 50 years. Antarc. Sci. 23, 461–468. 28. EPICA Community Members (2004). Eight glacial cycles from an Antarctic ice 25. Serrezer MC, Holland MM, Stroeve J (2007) Perspectives on the Arctic’s core. Nature 429, 623–628. Shrinking Sea-Ice Cover. Science 315 5818. 29. Barbraud C, Rolland V, Jenouvrier S, Nevoux M, Delord K, et al. (2012) Effects 26. Comiso JC, Parkinson CL, Gersten R, Stock L (2008) Accelerated decline in the of climate change and fisheries bycatch on Southern Ocean seabirds: a review. Arctic sea ice cover, Geophys. Res. Lett., 35. Mar. Ecol. Prog. Ser. 454, 285–307. PLOS ONE | www.plosone.org 9 January 2014 | Volume 9 | Issue 1 | e85285 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLoS ONE Pubmed Central

Emperor Penguins Breeding on Iceshelves

PLoS ONE , Volume 9 (1) – Jan 8, 2014

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1932-6203
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1932-6203
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10.1371/journal.pone.0085285
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Abstract

We describe a new breeding behaviour discovered in emperor penguins; utilizing satellite and aerial-survey observations four emperor penguin breeding colonies have been recorded as existing on ice-shelves. Emperors have previously been considered as a sea-ice obligate species, with 44 of the 46 colonies located on sea-ice (the other two small colonies are on land). Of the colonies found on ice-shelves, two are newly discovered, and these have been recorded on shelves every season that they have been observed, the other two have been recorded both on ice-shelves and sea-ice in different breeding seasons. We conduct two analyses; the first using synthetic aperture radar data to assess why the largest of the four colonies, for which we have most data, locates sometimes on the shelf and sometimes on the sea-ice, and find that in years where the sea-ice forms late, the colony relocates onto the ice-shelf. The second analysis uses a number of environmental variables to test the habitat marginality of all emperor penguin breeding sites. We find that three of the four colonies reported in this study are in the most northerly, warmest conditions where sea-ice is often sub-optimal. The emperor penguin’s reliance on sea-ice as a breeding platform coupled with recent concerns over changed sea-ice patterns consequent on regional warming, has led to their designation as ‘‘near threatened’’ in the IUCN red list. Current climate models predict that future loss of sea-ice around the Antarctic coastline will negatively impact emperor numbers; recent estimates suggest a halving of the population by 2052. The discovery of this new breeding behaviour at marginal sites could mitigate some of the consequences of sea-ice loss; potential benefits and whether these are permanent or temporary need to be considered and understood before further attempts are made to predict the population trajectory of this iconic species. Citation: Fretwell PT, Trathan PN, Wienecke B, Kooyman GL (2014) Emperor Penguins Breeding on Iceshelves. PLoS ONE 9(1): e85285. doi:10.1371/ journal.pone.0085285 Editor: Antoni Margalida, University of Lleida, Spain Received June 27, 2013; Accepted December 4, 2013; Published January 8, 2014 Copyright:  2014 Fretwell et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: Funding for this study came internally from BAS-NERC ecosystems programme. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. No current external funding sources for this study. Competing Interests: The authors have declared that no competing interests exist. * E-mail: ptf@bas.ac.uk obligate, the species is too clumsy to climb onto ice shelves and Introduction needs ice of a low freeboard to exit the ocean [2]. Of the 46 Recent studies suggest that emperor penguin populations will colonies presently known 44 breed on fast-sea- ice [13] (stable sea- decline in future decades due to climate change [1–6]. Current ice attached to the coast). Of the two remaining colonies, one is projections suggest that the world population will halve before recorded as breeding on rock and one on a frozen lake, both of 2052[3] with more northerly colonies, above 70uS being lost these colonies are small, one having a recorded population of 2900 entirely [6]. This has led the IUCN to re-list the species from pairs and the other 250 pairs [13] (the mean colony size is ‘‘Least Threatened’’ to ‘‘Near Concern’’ [7]. The primary reason approximately 5500 pairs). cited for this predicted decline is the species’ reliance on sea-ice, a In recent years satellite observations have improved our habitat that is expected to decrease in future years [8,9]. Sea ice is knowledge of the emperor penguins breeding distribution [14] important to the species in two ways; firstly as a breeding platform and population [13]. Here we report on newly discovered and secondly as a foraging environment. A decrease in sea-ice breeding behaviour in emperor penguins seen from satellite and distribution will negatively impact food webs [10], reducing aerial surveys. Four emperor colonies have been observed numbers of Krill (Euphausia superb), and the higher trophic levels which breeding on ice-shelves not sea-ice The first, discovered in feed on Krill such as glacial squid (Pleuragramma antarcticum); two species 2009[15]on the West Ice Shelf at the edge of Barrier Bay was a which compose the majority of the emperors diet [11]. A decrease small colony of that could have been judged an anomaly or a in food availability may negatively affect survival, breeding break off group from the larger West Ice shelf colony located success, recruitment and therefore population size. ,110 km to the north. However, since the discovery of the As a breeding platform, stable or ‘‘fast’’ sea-ice is required which colonies on the West Ice Shelf, three other, large colonies, have forms when the emperors arrive at their breeding locations (usually been found that are either permanently, or annually located on ice in April) and remains unbroken until the chick fledge (usually in shelves rather than on sea-ice. December). If the sea-ice breaks up too early in the season it will Whereas sea-ice is frozen sea-water, ice-shelves are floating result in high chick mortality [1–6], multiple years of poor sea-ice glacial ice that has flowed from the land into the sea; where the will lead to poor breeding success, population decline and eventual base of such glaciers breaks hydrostatic equilibrium, the ice-foot extinction of a colony [12]. The emperor penguin is a sea-ice detaches from the ground bed and the glacial ice floats. When a PLOS ONE | www.plosone.org 1 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves single glacier feeds into the sea a glacier tongue is formed, but group was located near the edge of the ice cliff of the West Ice around the Antarctic coastline it is more common for ice from Shelf. The birds had accessed the ice shelf via an ice gully several glaciers or ice-streams to merge to form an ice-shelf. At approximately 5km to the southeast. The colony has been their terminus ice-shelves can form ice cliffs, in some place over 60 observed in three subsequent years in the same position. The metres high, although a few tens of metres is more common. Ice presence of chicks at Barrier Bay confirms that this is a breeding creeks often indent the cliff face giving a potential route up onto location rather than a temporary site (Figure 1). the ice-shelf itself, or where ice shelves are ablating the ice cliff may The second colony identified on the top of an ice shelf is the be less steep. As sea-ice forms, local weather conditions mean it Shackleton Ice Shelf colony. This colony was first located in 2008 can be highly variable in extent and duration, and therefore highly [14] at 64.86uS, 96.02uE. The December 2008 position, found by susceptible to regional climate change [8]. Ice-shelves are less Landsat imagery and later confirmed by Very High Resolution dynamic, and are less susceptible to weather patterns and storm (VHR) satellite imagery (November 2009), was on sea-ice. The events, although cyclical calving events could pose a threat to colony comprised approximately 6,470 pairs [13]; satellite organisms located near the ice-cliff edge and over longer time observations confirmed that the breeding location remained periods ice-shelves can collapse catastrophically such as the well constant in 2008, 2009 and 2010. However, in 2011 it appeared documented break-up of the Larsen B Ice Shelf in 2002[16]. 15km to the south (64.98uS, 96.06uE) of its original location and It is at present unclear whether this behaviour of breeding on ice on top of the ice shelf. The access route to the top of the shelf was a shelves is a new phenomenon associated with recent climate gulley 3.4 km to the east. In 2012, the breeding location was the same as in 2011 (Figure 2). change, or one that has always existed but has not yet been documented. Models of how animals adapt to climatic change The third breeding location on top of an ice shelf is near the exist [17] and we examine how this phenotype plasticity fits into Jason Peninsula, at the northern limit of the Larsen C Ice Shelf. In those theories (see discussion). 1893, the explorer and sealer Carl Anton Larsen was the first to That emperor penguins can move their breeding site depending visit this area [18,19]. He reported on 4 December 1893 that ‘‘The upon ice conditions to a more stable location, including onto the kongepenguinerne (king penguin) are very numerous in those (ice) top of the ice-shelf itself, means new factors should be incorporated fjords’’ (ice creeks are a favoured breeding location of emperor into modelled population trajectories for this species. Whether penguin colonies). When recording this, his ship was located on such factors will provide temporary or permanent relief from the the northern side of what became known as the Larsen C Ice Shelf (noon position of 67.00uS, 60u.00W). At the time of this discovery impacts of climate change remains uncertain. The fact that emperors exhibit a previously unknown breeding little was known about emperor penguins and they were often behaviour, intimates that other less-well known species may also confused with the similar, but smaller king penguin (A. patagonicus), a species which Larsen would have been familiar with from his have similar unknown adaptive behaviours that may also offer temporary or permanent relief to the challenges of climate change. sealing trips to South Georgia. It is likely that Larsen’s sighting late in the breeding season indicated a colony in the vicinity. Although exhaustive satellite searches of the sea-ice in the area during Materials and Methods previous studies [14,15] were conducted, no colony was found. Observations However, in 2012, a further satellite survey for emperor colonies The first emperor colony found on an ice shelf was the Barrier was conducted along the edge of the Larsen C Ice Shelf. A Bay colony, 67.22uS, 81.93uE discovered in December 2009 [14]. medium sized colony was discovered on top of the shelf (at Some 295 chicks and a small number of adults were seen. The 66.08uS, 60.65uW). An aerial survey of the colony was undertaken Figure 1. Envisat images showing the sea-ice conditions in late March around the West Ice shelf where two emperor colonies are located (equivalent imagery for 2009 is not available). Darker areas denote poor sea-ice, grey shows thicker sea-ice and white indicates ice shelf. Note that the Barrier Bay colony has a permanent polynya while the West Ice shelf colony located on the sea-ice has thicker sea-ice at this time of year when the birds would be arriving in the area to breed (images courtesy of Polarview – www.polarview.aq). doi:10.1371/journal.pone.0085285.g001 PLOS ONE | www.plosone.org 2 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Figure 2. Shackleton Ice Shelf very high resolution satellite image. WorldView2 image (15 September 2012) showing the location of the Shackleton Ice shelf colony in 2012 in context with the ice edge. On this image the four main sub-colonies are clearly visible on top of the Shackleton PLOS ONE | www.plosone.org 3 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Ice Shelf around 5 km from the ice cliffs that form the edge of the ice shelf. The image data also clearly shows groups of penguins on their way to and from the ice edge, and the tracks they leave behind them. By marking these trails it is possible to assess where each group has come from and which direction it is heading. Interestingly at this site, the outgoing forages use a different route to the incoming penguins; on the way out they negotiate a large ice cliff. ICESAT data from the area suggest that the top of the ice sheet is 32–34 m high, the image shows no slope down to the cliff so the drop may be considerable (although there is evidence of large snowdrifts abutting the cliff). The incoming parties cannot negotiate the cliff and so take a 5 km longer route around the edge of the ice shelf until they can access the gentle slopes afforded by a number of ice creeks to the east of the colony. How the emperor penguins get down the ice cliff is, at present, unclear. doi:10.1371/journal.pone.0085285.g002 in early December 2012 (Figure 3) revealing that the colony above the ice cliff (Figure 5). At present no information is available comprised around 3,800 adult birds. Archival satellite imagery to suggest why the colony moved onto the shelf in this year. shows that it has been located on the ice shelf since at least 2008, the earliest imagery available for the area. The Antarctic Peninsula Analyses is one of the fastest warming regions [20] and has suffered To assess why the colony location had moved from sea-ice to significant ice shelf loss [21]. The sea-ice regime here has also been ice-shelf ENVISAT synthetic aperture radar imagery of sea-ice affected by climatic forcing and the birds may have moved from concentration was acquired of the Shackleton Ice shelf colony (for the sea-ice creeks to the top of the ice shelf. Exactly how the birds which the most data existed) several times over the course of the access the shelf is unclear but it appears that they climb the low ice breeding season. The imagery from March, when adults start to cliff (Figure 4). King penguins climb up dry glaciers in warm return to their breeding location [22], shows that in 2008, 2009 weather to stay cool; perhaps the less agile emperor is also able to and 2010 the sea-ice concentration at the initial site was dense and climb slopes, particularly where ice shelves weather and ablate the was sufficiently stable for the penguins to access the location steepness of the shelf face. (Figure 6). But in 2011 and 2012, the sea-ice did not form until Finally, a colony was sighted on top of an ice shelf at the early- to mid-April. The birds therefore chose a site on top of the Ruppert Coast colony. This colony was only discovered in 2010 ice shelf in years when sea-ice formed late. The birds show when it was located on the sea-ice under the ice cliffs of the remarkable fidelity to the site, changing their breeding platform in Nickerson Ice Shelf at 75.38uS, 143.35uW. Satellite imagery shows preference to changing the breeding location when April sea-ice that in 2008, 2011 and 2010 (no images from 2009 are available) conditions become unsuitable. the colony was located on the sea-ice at 75.38uS, 143.28uW, but in To test whether the presence of colonies that have been found 2012 (17/10/2012) it had moved onto the edge of the ice shelf on ice-shelves was linked to environmental conditions, three Figure 3. Emperor penguins on the edge of the Larsen Ice Shelf near the Jason Peninsula late in the breeding season. The larger group is on the ice-shelf, the smaller group has moved onto the fast-ice; earlier in the season data from QuickBird1 satellite imagery shows that the whole colony was located on the ice-shelf. Note the ice cliff which is probably an insurmountable barrier to the adult emperor penguins. No evident route to the colony was determined from the images. (Photo Ian Potten). doi:10.1371/journal.pone.0085285.g003 PLOS ONE | www.plosone.org 4 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves PLOS ONE | www.plosone.org 5 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves Figure 4. A and B; maps showing location of the Jason Peninsula colony. C: Quickbird1 image (12 Sept 2012) showing the main Jason Peninsula emperor penguin colony in relation to the ice-shelf and sea ice edge. D: Emperor penguins (small black dots) on their way to or from the breeding colony onto of the sea-ice. They have to climb up or down a small ice cliff, which shows up as white in this image. To the left of this cliff is ice shelf, while the ridged area to the right is fast-ice. In this image emperors can be seen on the ice shelf (a long line in upper left and parallel to the cliff face) and the cliff (shorter linear group at middle bottom and perpendicular to the cliff face). The height of this ice cliff is presently unknown but based on the size of the penguins in the image it may be only a few metres high. doi:10.1371/journal.pone.0085285.g004 environmental variables were assessed at the four sites and catalogue number 101001000A9A8B00 November 12th 2009 ), compared with values for other emperor penguin colony locations a possible response to poor sea-ice earlier in the season. A similar (Figure 7). Autumn (March/April) sea-ice concentration was behaviour has been observed at the Mertz Glacier colony which is also located in an area that has a high mean temperature (Andre´ modelled using synthetic aperture radio imagery from the Polarview website (http://www.polarview.aq/), mean temperature Ancel pers coms.). This behaviour at these other colonies suggests that breeding on ice-shelves is only one of several possible was assessed using the RACMO region climate model [23] and adaptations that could be employed by emperor penguins when latitude using the recent calculation of the circumpolar emperor sea-ice conditions are poor; others include moving onto land (for penguin population [13]. example Dion Islands). Of the other warmer sites the Snow Hill Island colony has not only the warmest mean temperature but is Results and Discussion also is the highest latitude, although it has a reasonable high mean Of the four colonies described here, the three that have been sea-ice concentration. Bowman Island has the third highest mean found breeding on ice shelves in multiple years could be described temperature and the fourth lowest sea-ice concentration. These as located in marginal conditions. The Shackleton Ice Shelf and two must be considered some of the most marginal and potentially Barrier Bay sites have the lowest mean autumn sea-ice concen- vulnerable of emperor breeding locations as neither colony has the trations of any colonies and both these and the Larsen ice-shelf option of moving onto floating ice-shelves as there are none in the colony are in the most northerly part of the emperors range and nearby locality and neither has it shown evidence of breeding on have higher-than-average mean-temperature regimes. Three other icebergs. colonies have mean annual temperatures higher than the Larsen The Ruppert Coast colony that has been found located on the colony; Smyley Island, Bowman Island and Snow Hill Island. On edge of an ice shelf in one year is neither in a warm or poor sea-ice Smyley Island in 2009 the colony was observed by QuickBird location; as yet we have no explanation of why this colony moved satellite imagery breeding on top of an iceberg (QuickBird to a more elevated location. Figure 5. QuickBird 2 very high resolution satellite image of the Ruppert Coast emperor penguin colony(17 October 2012) including part of the Ruppert Coast and Nickerson Ice Shelf, it clearly shows the emperor penguin colony located on the higher ice shelf. Access to the main colony seems to be by a shallow ice ramp north and west of the present location. Brown guano stains mark the previous colony site approximately half a kilometres northeast, and to the west, on the sea-ice is a smaller subgroup of penguins. doi:10.1371/journal.pone.0085285.g005 PLOS ONE | www.plosone.org 6 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves th Figure 6. Sea-ice concentration around the Shackleton Ice Shelf for the time period 2007 to 2012, each from the 20 of March. White shading denotes thick sea-ice; blue, thinner sea-ice; black, open water. The red dot shows the location of the breeding colony identified from QuickBird VHR imagery (images courtesy of Polarview/University of Bremen). doi:10.1371/journal.pone.0085285.g006 Only a relatively small number of emperor colonies have been shelves, as reported here, has only been reported once at a small studied across Antarctica [1,12,22,24], with the longest study colony in East Antarctica [15]. That this behaviour is not the based at Pointe Ge´ologie, which has been continually monitored exception but is apparently more common among emperor since the 1950s [1,4,5,24]. The behaviour of breeding on ice- penguins is a surprising result. The reasons why this behaviour Figure 7. Marginality. Histogram of three parameters at emperor penguin breeding colonies: blue bars represent mean March/April sea-ice concentration, red bars are latitude and green are mean temperature. Colonies are ranked from left to right with lowest sea-ice concentrations to the left. The four colonies mentioned in this paper are named in bold. Dashed lines in blue, red and green denote the mean of the three parameters for all colonies. Shackleton Ice shelf and Barrier Bay colonies are in locations that have the lowest mean autumn sea-ice concentrations. The Larsen ice shelf colony has slightly lower than average sea-ice concentrations, but its latitude and mean annual temperature are well above average. The colony on the far left, Dion Islands, marked in red is believed to have declined and ceased to exist following recent climate change (temperature rise and sea- ice loss) on the Antarctic Peninsula. This previously occupied site is included to give an indication of the current breeding limits. These parameters give no indication of why the Ruppert Coast colony, found breeding on the ice shelf in only one year, relocated onto this ice shelf in 2012. Mean sea- ice concentration (blue) is recorded as a percentage for March/April when emperors prospect and recruit at breeding sites. The figures are calculated using synthetic aperture radar measurements for all dates in these two months for the years 1998–2007. Latitude (red) is the latitude of the colony location from Fretwell et al. 2012 and Wieneke 2012, with the addition of the newly found Larsen Ice Shelf colony described in this paper. Mean temperature is based on a yearly mean for 2000–2004 based on the RACMO climate model. doi:10.1371/journal.pone.0085285.g007 PLOS ONE | www.plosone.org 7 January 2014 | Volume 9 | Issue 1 | e85285 Emperor Penguins Breeding on Iceshelves has not been recorded before are unclear, possible explanations For emperor penguins, the loss of the sea-ice as a breeding include: platform is not the only consequence of a warming environment. Factors, such as changes to food webs [10,29] and increased 1. The phenomenon may be recent phenotypic plasticity as predation and competition [12] will also affect breeding success regional climate change affects parts of the Antarctic coastline. survival rates and other demographic parameters in areas that 2. Most previous study-sites are not located at ice-shelf breeding experience regional warming. Additionally, there are several colonies where this behaviour is exhibited. negative factors that could potentially result from breeding on 3. There have been no large scale systematic searches for ice shelves, including the lack of shelter and exposure to katabatic emperors on ice shelves (although many flights and surveys winds, lack of fresh snow in areas where increased wind speeds have overflown iceshelves). scour the surface and a risk from calving ice fronts. How great these risks are and how much of an advantage or disadvantage Visser [17] has proposed a number of possible adaptations to breeding on ice-shelves proves to be for this species has yet to be climate change in birds, including phenotype plasticity, which quantified. This new discovery also leads to a number of other includes changes in breeding behaviour. One special case of potential behavioural questions. For example: How do emperors phenotype plasticity noted in the work is that of ‘‘learning’’ where access the ice shelves? Does the breeding cycle differ in locations animals can adapt to climate change if they learn from their such as at the Larsen colony where breeding on ice-shelves has experiences. Whether the adaptation of emperor penguins become the norm? What is the energetic cost of scaling the ice- breeding on ice-shelves is learnt, or inherited behaviour is at front? Such questions will be important future topics of research. present unclear; the Larsen and Barrier Bay colonies seem to be Currently, sea-ice conditions and their predicted decline are one permanently located on the shelf, but the Shackleton colony moves of the key inputs into models that suggest large decreases in there only when sea-ice conditions in April dictate. One aspect of emperor penguin numbers. Therefore, the suitability of ice-shelves Visser’s work that must be considered is that it concentrates on versus sea-ice as a breeding platform for emperors urgently needs individual nesting birds rather than colonial species. Colonial quantifying. Future research efforts need to assess which colonies species, especially emperor penguins, seem to move en-mass to could potentially move to ice-shelves and whether this newly new locations, although how this decision is made is unclear. The described behaviour is a temporary or partial solution for coping previous work may not therefore prove an ideal model for with future climate change. Emperors are often portrayed as a assessing how colonial nesting sea-birds may adapt to climate barometer for the ecosystem, that is, a ‘‘canary in the coalmine’’ change. for species more difficult to study. This previously unknown and The ability of emperor penguins to change their breeding surprising behaviour recorded in such an iconic animal suggests platform when fast ice conditions deteriorate may be an important that other species may also be capable of unpredicted or unknown adaptation that could help the species survive in a warming behavioural adaptations that may also increase their survival in a environment. Although regional warming has led to loss of ice- future warming world. shelves around the Antarctic Peninsula [21] ice-shelves are less sensitive to a warming environment and react to warming on Author Contributions slower timescales than sea-ice, the extent, stability and seasonality of which can change rapidly with warming temperatures as Conceived and designed the experiments: PTF PNT BW GLK. Performed already seen in the Arctic [25,26,27,28] and in the west Antarctic the experiments: PTF. Analyzed the data: PTF BW. Contributed reagents/ Peninsula [8]. materials/analysis tools: PTF. Wrote the paper: PTF PNT BW GLK. References 1. Barbraud C, Weimerskirch H (2001) Emperor penguins and climate change. 12. Trathan PN, Fretwell PT, Stonehouse B (2011) First Recorded Loss of an Nature 411, 183–186. Emperor Penguin Colony in the Recent Period of Antarctic Regional Warming: 2. Ainley DG, Clarke ED, Arrigo K, Fraser WR, Kato A, et al. (2005) Decadalscale Implications for Other Colonies PLoS ONE 6; e14738: doi:101371/journal- changes in the climate and biota of the Pacific sector of the Southern Ocean, pone0014738. 1950s to the 1990s. Ant Sci 17; 171–182. 13. Fretwell P T, LaRue MA, Morin Pl, Kooyman GL, Wienecke B, et al. (2012) An 3. Ainley D, Russell J, Jenouvrier S, Woehler E, Lyver P, et al. (2010) Antarctic Emperor Penguin population estimate: The first global, synoptic survey of a penguin response to habitat change as Earth’s troposphere reaches 2uC above species from space. 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