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Trends in the Breeding Population of Adélie Penguins in the Ross Sea, 1981–2012: A Coincidence of Climate and Resource Extraction Effects

Trends in the Breeding Population of Adélie Penguins in the Ross Sea, 1981–2012: A Coincidence of... Measurements of the size of Ade´lie penguin (Pygoscelis adeliae) colonies of the southern Ross Sea are among the longest biologic time series in the Antarctic. We present an assessment of recent annual variation and trends in abundance and growth rates of these colonies, adding to the published record not updated for more than two decades. High angle oblique aerial photographic surveys of colonies were acquired and penguins counted for the breeding seasons 1981–2012. In the last four years the numbers of Ade´lie penguins in the Ross and Beaufort Island colonies (southern Ross Sea metapopulation) reached their highest levels since aerial counts began in 1981. Results indicated that 855,625 pairs of Ade´lie penguins established breeding territories in the western Ross Sea, with just over a quarter (28%) of those in the southern portion, constituting a semi-isolated metapopulation (three colonies on Ross Island, one on nearby Beaufort Island). The southern population had a negative per capita growth rate of 20.019 during 1981–2000, followed by a positive per capita growth rate of 0.067 for 2001–2012. Colony growth rates for this metapopulation showed striking synchrony through time, indicating that large-scale factors influenced their annual growth. In contrast to the increased colony sizes in the southern population, the patterns of change among colonies of the northern Ross Sea were difficult to characterize. Trends were similar to southern colonies until the mid-1990s, after which the signal was lost owing to significantly reduced frequency of surveys. Both climate factors and recovery of whale populations likely played roles in the trends among southern colonies until 2000, after which depletion of another trophic competitor, the Antarctic toothfish (Dissostichus mawsoni), may explain the sharp increasing trend evident since then. Citation: Lyver PO, Barron M, Barton KJ, Ainley DG, Pollard A, et al. (2014) Trends in the Breeding Population of Ade´lie Penguins in the Ross Sea, 1981–2012: A Coincidence of Climate and Resource Extraction Effects. PLoS ONE 9(3): e91188. doi:10.1371/journal.pone.0091188 Editor: Hans-Ulrich Peter, Institute of Ecology, Germany Received November 1, 2013; Accepted February 10, 2014; Published March 12, 2014 Copyright:  2014 Lyver 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: This work was primarily funded by New Zealand’s Foundation for Research, Science and Technology grants (C09527; C09X0510) and Ministry of Science and Innovation project (C01X1001; CONT-21216-BKBN). Funding for DA, AP, and GB came from the National Science Foundation (OPP 0944411). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Two co-authors work for commercial companies, H. T. Harvey & Associates Ecological Consultants and Bartonk Solutions. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. * E-mail: lyverp@landcareresearch.co.nz Annular Mode), are expressed through the physical environment. Introduction Examples include changes in sea-ice conditions such as concen- The underlying factors most likely to limit the abundance of tration, extent and thickness, air temperatures, winds, sea surface breeding seabirds in a region are prey or nesting space availability temperatures (SST) and precipitation (see Ainley et al. [3] and [1]. These effects are manifest in key demographic rates such as references therein). In the case of high latitude Antarctic penguins, age-specific survival, dispersal and proportion breeding. This is the issue is related to a sea-ice optimum lying between extremes especially so for central-place foragers like Antarctica’s ‘‘true’’ that can affect them in different ways [4] (see also Jenouvrier [5] pack-ice penguins, Emperor (Aptenodytes forsteri) and Ade´lie for a general application of climate optima to avian trends), as (Pygoscelis adeliae) penguins, which breed gregariously in large indicated empirically within the palaeoecological and ecological colonies [2]. The inability of these penguins to forage across vast records of Emperor and Ade´lie penguin populations [6], [7], [8], distances means that they are influenced to a greater degree than [9], [10]. A switch of the AAO in the mid-1970s from variable, volant species (e.g. albatrosses Diomedea spp.) by the local habitat negative-to-positive on a decadal scale, to almost always positive and resources and by changes in conditions and prey stocks. thereafter brought changes in winds and sea ice [11] and in turn Population responses of penguins to changing ecosystems can be affected pack-ice penguin populations [3], [6], [7]. complex. Spatio-temporal variation in climatic variables resulting Climate change, however, by no means is the total story. from phenomena such as long-term climate change, or shorter- Significant changes in Ade´lie penguin numbers could warn of term decadal atmospheric variation, i.e. factors related to the changes in the abundance of their prey and/or structure and Southern Oscillation and Antarctic Oscillation (AAO, or Southern function of the marine ecosystem owing to other factors [12]. PLOS ONE | www.plosone.org 1 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Depletion of whales and demersal fish has been associated with nests, though some expressed nervousness (a portion waving their flippers, P. Wilson pers. obs.; Brian Karl pers. obs.). Prior to 2006, large-scale changes in abundance of Antarctic penguins and other diving species, i.e. seals (Mirounga, Arctocephalus) and shags photographs were taken with a Pentax 645 medium format black and white film-back camera. This unit was upgraded in 2006 to a (Phalacrocorax spp.) [13], [14], [15], [16], [17]. In the Ross Sea, the dramatic increase in Ade´lie penguin numbers from the mid- Hassleblad H1D 22 MP medium-format digital camera, which was then replaced with a Canon EOS 1DS Mark III camera for 1970s to the early 1980s, followed by slow decline, has been correlated with the depletion by commercial whaling and then the 2011/12 season. We used photographs that were taken each year as close as recovery of Antarctic minke whales (Balaenoptera bonaerensis)in International Whaling Commission Areas V and VI [18], [19]. possible to 1 December (range of dates: 25 November to 8 December) each season. This is a date on which the colony Ross Sea penguins and minke whales feed on the same prey [20] and the penguins have since been found to begin their wintering population, owing to its seasonal dynamics, was represented almost entirely by one member of each penguin pair incubating its mode in the area where most of this whaling occurred: waters eggs, and minimal numbers of non-breeders [12]. Even though north of Victoria Land [21]. our surveys were conducted within a two week window, it is Reliable repeated assessments over the long term are therefore possible that phenology, monitored on the ground at Ross Island crucial for understanding how these and other factors influence colonies, still accounts for a small proportion of the inter-annual breeding population sizes and dynamics for high latitude penguins, variation we observed. Census data from surveys conducted prior and hence for informing management. The Ade´lie penguin is one to 1981 were not used because they were ground-based and only of the species monitored by the Commission for the Conservation for two of the three colonies – Cape Royds and Cape Bird. The of Antarctic Marine Living Resources (CCAMLR) as part of its population data from the years 1998–2012 are presented here for CCAMLR Ecosystem Monitoring Program (CEMP) to potentially the first time. For a full description of survey methods (e.g. detect anthropogenic effects on Antarctic marine ecosystems [22]. prioritization, location and flight approaches for colonies, and In the Ross Sea sector of the Southern Ocean, Ade´lie penguins camera specifications) please refer to references [22], [24] and breed over a latitudinal range of 1200 km, from the Balleny [25]. Operational permits were approved and issued by New Islands (Buckle Island, 66u 509 S) north of the Ross Sea to Ross Zealand’s Ministry of Foreign Affairs and Trade under the Island (Cape Royds, 77u 339 S) in the south (Fig. 1) and therefore Antarctic (Environmental Protection) Act 1994 and Landcare may be exposed to a range of environmental conditions and Research’s Animal Ethics Committee 2005 and 2010 respectively habitats, e.g. abyssal ocean, continental slope and shelf ecosystems. (0509/01 and 10/09/01). Data is available upon request via: The objective of this study, therefore, was to add to the long-term http://www.landcareresearch.co.nz/resources/data/adelie-census- record and measure variation in the size of the Ade´lie penguin data). breeding populations in subregions of the western Ross Sea during the period 1981–2012. Owing to the infrequent surveys along the Manual and Semi-automated Mapping and Counting of northern Victoria Land coast after the mid-1990s, we focused our assessment primarily on the annual or near-annual surveys of the Colonies southernmost cluster (and likely metapopulation; see [23]) of Prior to 2006, film negatives were developed in a dark room, Ade´lie penguin colonies: three colonies on Ross Island [Cape and the resulting photographs of the colony were printed and manually joined together. Once a mosaic of the colony was Royds, Cape Bird (North, Middle and South), Cape Crozier (East and West)] and one on Beaufort Island, about 20 km north of constructed, the appropriate photographs were enlarged and each territory occupied by a penguin counted by marking it with a dot Cape Bird. We examined a range of diagnostics such as means and variations in colony size, rates of change in abundance with time to ensure that each was counted only once. This method of counting was slow, and it was difficult to verify counts at a later (annual growth rates), and evidence of trends and cycles. To conclude we offer hypotheses that might explain the trends and stage. However, the method had the benefit that a physical record was kept for each census. changes in colony sizes observed over the past three decades. From 2006, the colony images were captured digitally but the photographs were still processed and penguins counted manually. Methods In 2010, semi-automatic penguin counting software was developed Census Surveys of Colonies so that colony mapping, counts and verification of counts could occur on the computer screen [26]. High angle oblique aerial photographs of Ade´lie penguin adults occupying nesting territories at colonies along the Victoria Land coast and offshore islands were acquired for the period 1981–2012 Time-Series Analysis (see Taylor and Wilson [24](1990) and Wilson et al. [25] (2001) for The Cape Bird totals are the sum of counts of 3 partitions of the discussion of trends from 1959 to 1997, based on both aerial and colony and the Cape Crozier counts are the sum of 2 partitions of ground counts, as well as the discovery of 11 previously unreported that colony, but in 3 different years counts from one of the three breeding colonies). We define ‘‘nesting territories’’ as sites Cape Bird partitions were not available. To avoid biasing the total occupied and defended by both breeding and non-breeding adults colony count towards zero these missing values for Cape Bird were (see below). Colonies on Ross Island (Cape Royds, Cape Bird and interpolated by fitting a cubic smoothing spline to the colony Cape Crozier) and Beaufort Island (Fig. 1 – herein referred to as partition time series using the ‘‘zoo’’ package in the statistical the southern metapopulation) were photographed annually from a software ‘‘R’’ [27]. Variation in counts within a colony was helicopter flying at an altitude of 2000–2500 feet (610–765 m) assessed by calculating the standard deviation of the logarithmic above ground level. Colonies along the northern Victoria Land transformation of the counts (s) [28]. coast (Fig. 1) were photographed only occasionally after the mid- Visual inspection of the colony time series indicated a potential 1990s, from the open paratroop doors of a C-130 Hercules flying change point in the trends in counts of southern colonies around at a minimum altitude of 2,500 feet a.g.l. Observations from the the years 2000–2001. To assess differences in trends 1981–2000 vs ground showed that over-flights of helicopters and C-130 aircraft 2001–2012, a generalized least squares model was fitted to each of at altitudes of at least 2000 feet a.g.l. did not force birds to leave the log -transformed Ross Island colony counts with first-order PLOS ONE | www.plosone.org 2 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Figure 1. Distribution and size categories (based on 1981–2012 means) of Ade´lie penguin colonies from the western Ross Sea, Antarctica. doi:10.1371/journal.pone.0091188.g001 correlation (AR(1)) in the error term to account for the inherent the confidence intervals of the mean correlation coefficient were dependence of a count in one year on the count last year. Two estimated using the bootstrap algorithm of Bjørnstad et al. [30] models were fitted for each colony, one with a linear trend with (1999), implemented in the ‘‘ncf’’ package for the statistical time across all years (1981–2012), and one with different linear software ‘‘R’’. trends in the periods 1981–2000 and 2001–2012, in which the two periods were specified using dummy variables. The best fitting Results model out of the two was selected using the Akaike Information Size and Variation in Breeding Pairs of Ade´lie Penguin Criteria corrected for small sample sizes (AICc). Phase plots of current colony counts against lagged counts (t-1 vs Colonies in the Ross Sea t; both log -transformed) were constructed as a visual means of During our 30-year survey period 855,625 pairs of Ade´lie assessing density dependence [32]. To identify any periodicities or penguins on average held nesting territories just prior to hatching density dependence (Year 1 to Year 10) in the time series of colony at colonies in the western Ross Sea (Table 1). Around a quarter counts, autocorrelation functions (ACF) and partial rate correla- (28%) of this number breed as part of the southern metapopulation tion functions (PRCF) were estimated for each of the three Ross with two-thirds (64%) of those birds concentrated at Cape Crozier Island colonies [29]. The significance of the correlations was tested (Table 1). The variation (or amplitude, s-value) in annual colony with Bartlett’s band 6 2/!n, where n is the length of time series. size variations across colonies in this population was similar Spatio-temporal synchrony between annual colony growth rates (range = 0.11 to 0.15; Table 1). The s-values indicate that the (r = log (N ) – log (N )) was assessed by calculating cross- average ‘‘peak to trough’’ ratio of counts is around one-third to t e t+1 e t correlation coefficients (r ) between all pairs of the Ross and one-half an order of magnitude (s = 0.35 is equivalent to one order i,j Beaufort island colonies. The mean correlation coefficient was of magnitude variation) indicating a lack of cycles in the data [27]. calculated to quantify spatial synchrony across colonies in the Counts of Ade´lie penguin breeding pairs in the northern Victoria southern metapopulation. Because of autocorrelation in the data, Land population over the last 20 years have been infrequent so the PLOS ONE | www.plosone.org 3 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends variation, although also quite similar across colonies (range = 0.09 Discussion to 0.22; Table 1), needs to be interpreted with caution. Status and Trends in the Ross Sea Ade´lie Penguin Population Trends in Size of Ade´lie Penguin Colonies in the Ross Sea A regression model with two separate trend lines fitted the The aerial survey data reported here provide the most recent counts of Ade´lie penguin breeding pairs in the Ross Sea, extending colony count data best for the Beaufort Island, Cape Bird and Cape Crozier colonies, but not for Cape Royds, where a single in time by 2.5 decades one of the longest monitored Antarctic penguin populations. In the last four years, the numbers of Ade´lie trend line was selected (Table 2). Our model indicated a generally decreasing trend in the number of breeding pairs at the Beaufort penguins, at least in the southern Ross Sea, have grown to their highest levels since aerial counts began (1981), as well as since all Island, Cape Bird and Cape Crozier colonies between 1981 and 2000, then an increasing trend from 2001 to 2012 (Table 2; Fig. 2). counts began in 1959 (cf. [23]). Even so, our mean count of 855,625 breeding pairs for the Ross Sea was still lower than the The small Royds colony appeared to be stable until it decreased sharply in 2000 and 2001, followed by a period of no growth or mean count of 938,877 breeding pairs reported by R.H. Taylor during the 1980s (pers. comm. in Woehler [31] 1993). This slight growth beginning in the last two years. In aggregate, this difference can be potentially explained by the infrequent surveys of metapopulation had an average negative per capita annual growth rate of 20.019 over the 1981–2000 period followed by an average Victoria Land colonies, where in the past approximately 75% of the Ross Sea population have bred, over the last 25 years when positive per capita annual growth rate of 0.067 over the 2001– 2012 period, reflecting primarily the pattern in the larger colonies numbers were potentially substantially lower than in the 1980s. We do not report numbers from the four Victoria Land colonies (not Royds). The two larger colonies had close to twice (1.8 times) the number of birds in 2012, than the 30-year average (Table 1). west of Cape Adare (Fig. 1) (no more than ,3,000 pairs [12], Lyver unpubl. data). There was synchrony between colonies in annual changes in size through this period with a common low point in counts around The most current assemblage of counts indicates about 38% of Year 2001 for all colonies (Fig. 2). the circum-Antarctic Ade´lie penguin population breeds in the Changes in abundance of Ade´lie penguins at seven colonies of Ross Sea [12]. Coupled with observed increases in the Ross Sea northern Victoria Land for which we had data from six or more over the last decade, expanding distributions in east Antarctica surveys over the 30 years were variable. There appeared to be [32], and decreases in colonies in the northern Antarctic Peninsula initial stability or perhaps decrease through 1991, but thereafter, region but increases in the south [16], this percentage may still be with sparse counts, no clear trend was evident (Table 3; Fig. 3). approximately correct. A large concentration (historically ,47% of the Ross Sea population) in the extreme northern Victoria Land focuses around four colonies: Possession Island, Foyn Island, Colony Size Regulation Downshire Cliffs, and Cape Adare (Fig. 1). We have limited The auto-correlation functions (ACF) for log -transformed information about recent trends in these colonies, although some colony sizes showed no evidence of cycles in the time series, with of them might be space-limited. It is likely that these large significant lags occurring only at 1 year or both years 1 and 2, concentrations occur where they do because of nesting habitat though the length of the time series is relatively short for such availability, proximity to persistent polynyas where open water detection. The slow decay of the ACF to negative values at high facilitates access to prey [12], and proximity to the highly lags is indicative of a trend in the data (as discussed in the previous productive Ross Sea Slope Front [33]. section). The partial rate correlation functions (PRCF) for the rates The presence of unoccupied sub-colony mounds with ample of change versus log -transformed colony size all showed a supplies of pebbles for nest-building indicates that the colonies on significant negative correlation at lag 1 indicative of direct density Ross Island are not space-limited. However, recent recession of ice dependence in the number of pairs returning to the colony each fields on Beaufort Island have resulted in more nesting habitat, year. This indicates that high colony counts in one year tend to meaning that recruits within this metapopulation no longer have result in lower growth rates to the following year, and vice versa: to emigrate to the Ross Island colonies to find nesting space [23]. low colony counts in one year tend to result in higher growth rates Therefore, only recently has Beaufort been able to grow. We to the following year (Fig. 4). There were also significant negative suggest that the numbers breeding in the southern colonies are correlations between rates of change and colony size 8 years now more likely to be limited by food accessibility, mediated in previously for Cape Royds and Cape Crozier. Phase plots for Cape Royds and Cape Crozier showed relatively small back-and- part by environmental stochasticity (especially fast ice cover) in the case of Cape Royds and perhaps Cape Bird [34] and by inter- and forth fluctuations about the mean colony size throughout the intra-specific competition at Cape Crozier and Beaufort Island 1980s and 1990s, indicative of direct density dependence, followed [20], [23], [35]. by larger variation in colony sizes from the Year 2000 on, indicating looser regulation. The phase plot for Cape Bird showed consistent clockwise orbits, indicative of ongoing delayed density- ´ Drivers of Adelie Penguin Abundance in the Ross Sea dependent feedback on colony size. The similar low level of amplitude associated with colony size variation across the southern metapopulation indicates that Synchrony in Annual Colony Growth Rates colonies could be responding in concert to a single or multiple Annual colony growth rates (r) for the southern population common drivers (except for Royds during and after the mega- showed a striking level of synchrony through time (Fig. 5). This iceberg B-15 era; see below). This is supported by the high level of was confirmed by a high mean (cross-) correlation for the Ross and synchrony and correlation in annual growth (Fig. 5). The relationship between annual colony growth rates and size indicates Beaufort island colonies of 0.59, with a 95% (bootstrapped) confidence interval of 0.35–0.77. The lowest levels of synchrony that a form of density dependence could be influencing colonies, supported by the fact that initially recent growth at Beaufort was were between Beaufort Island and the other colonies (R = 0.35– 0.59). Synchrony between the other three colonies (Cape Royds, due to infilling of the colony followed by expansion into new Cape Bird and Cape Crozier) was higher, with correlation breeding habitat [33]. Since currently there is ample space for coefficients of 0.68–0.77. additional growth at all these colonies (see [23]), competition for PLOS ONE | www.plosone.org 4 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Table 1. Mean colony counts of nesting territories (with colony counts from Ross Island 2012 for comparison) and s, a measure of the amplitude of colony size variations (n is the total number of counts per colony), for colonies in the southern Ross Sea metapopulation and along the Victoria Land coast between 1981 and 2012. Colony Mean colony count (Colony counts 2012) sN n contiguous Ross Island metapopulation Cape Royds 2,825 (3083) 0.11 30 30 Cape Bird 43,321 (75,696) 0.13 30 30 Cape Crozier 153,632 (272,340) 0.15 28 28 Beaufort Island 39,391 0.13 17 9 Victoria Land Franklin Island West 60,540 0.11 7 2 Franklin Island East 1,110 0.12 8 2 Inexpressible Island 24,450 0.09 9 2 Terra Nova Bay 11,234 0.13 9 2 Wood Bay 1,890 0.13 8 2 Cape Anne 268 0.22 6 1 Coulman Island South 17,991 0.09 6 4 Coulman Island Middle 4,325 0.11 9 5 Coulman Island North 1,694 0.10 8 4 Cape Jones 153 0.14 6 2 Mandible Cirque 16,837 0.10 3 2 Cape Phillips 3,921 0.08 4 3 Cape Wheatstone 2,746 0.18 6 3 Cape Cotter 38,252 0.16 8 3 Cape Hallett 42,628 0.14 14 8 Foyn Island 30,494 0.12 6 1 Possession Island 111,306 0.15 3 1 Downshire Cliffs 19,617 0.12 5 2 Cape Adare 227,000 0.09 4 1 doi:10.1371/journal.pone.0091188.t001 food or food availability is the most likely variable affecting birds’ remaining in place in McMurdo Sound for most of the period body condition and subsequent survival or decision whether to 2001–2005; besides nest desertions, many adults eventually return to breed in the following year. emigrated to Cape Bird [40]. Thus, recovery of the Cape Royds colony has been slow, showing positive signs only in the last couple of years. In contrast, the colonies at Beaufort, Bird and Crozier, Effects of Physical Changes in the Penguins’ Environment which were less affected by the increased sea ice, except in the Among the possible common drivers is sea-ice variation, with initial iceberg year, subsequently grew throughout the remaining the mega-icebergs showing this quite well at the local, mesoscale. mega-iceberg era up to the present. The depression in abundance of Ade´lie penguins in the southern The effects of ice bergs and the altered sea-ice regime were not Ross Sea population in 2001 was a common low point coinciding confined just to the southern Ade´lie penguins. B-15A and C-16 with the arrival of the giant icebergs B-15A and C-16 in January presence resulted in an initial decrease in Beaufort Island and 2001, and which remained in place until winter 2005. These Cape Crozier emperor penguins, followed by slow recoveries still icebergs, as well as B-15B, resulted in a one-season reduction in ongoing [41], [42] (Ballard et al. unpubl. data). The extensive fast primary production in the Ross Sea polynya, 2000/01 [36], [37], ice that remained in McMurdo Sound 2001–2005 resulted in a as well as an alteration of surface circulation [38]. The calving of depression in Weddell seal (Leptonychotes weddelli) numbers, but an even larger iceberg in 2002/03, C-19, also led to a one-season which recovered entirely once the icebergs departed and annual decrease in production (owing to more sea ice, and less ocean fast ice returned [43]. exposed to sunlight; [39], C. Smith, unpubl. data). While grounded, B-15A and C-16 prevented the wind from blowing Sea-ice cover at the larger scale can also affect Ade´lie penguins in a number of ways. A previous study analysing trends up to 1998 sea ice from the southwestern Ross Sea northward, except in 2003 when winds were particularly strong. Lots of sea ice decreased demonstrated a correlation between declines in the southern access to the ocean and food [4], [9]. colonies 4–5 years after anomalously extensive sea ice in the Ross Many Ade´lie penguin adults failed or abandoned breeding Sea sector of the Southern Ocean [25]. Those authors hypoth- attempts early in the breeding season in the initial year of the B- esized that juvenile Ade´lie penguin survivorship decreased in years 15A and C-16 iceberg groundings (2001/02). In the case of Cape when extensive sea ice carried the penguins well beyond the Royds, conditions were especially daunting with 70 km of fast ice productive feeding grounds that lie south of the Southern PLOS ONE | www.plosone.org 5 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Table 2. Summary of trend models for Cape Royds, Cape Bird and Cape Crozier (Ross Island) and Beaufort Island colony counts (log -transformed) with predictor units in years from 1981 to 2012. Best model (1 or 2 Trend 1981–2000 slope estimate Trend 2001–2012 slope estimate Colony linear trends) (std error estimate) (std error estimate) Cape Royds 1 20.0085 (0.00797) Cape Bird 2 20.0245 (0.00862) 0.0755 (0.01523) Cape Crozier 2 20.0223 (0.00784) 0.0981 (0.01213) Beaufort Island 2 20.0214 (0.01357) 0.1028 (0.03318) Values in bold text indicate statistical significance of the estimated slope parameter (r = per capita annual growth rates) at P,0.05. doi:10.1371/journal.pone.0091188.t002 Boundary of the Antarctic Circumpolar Current (SBACC). If the during the breeding season at least to a point, after which further winter-sea-ice extent in the Ross Sea sector regularly extended polynya growth is neutral to penguin well-being. beyond the SBACC then natural growth rates of Ade´lie penguin colonies could be affected, given that sea-ice extent has been Effects of Biological Changes in the Penguins’ growing in the Ross Sea sector, including more years of ice Environment extending north of the SBACC [44]). The sea-ice season and The more favorable polynya behaviour also likely played a large-scale extent in the Ross Sea region has increased by 3 complex role in trends through the 1990s [3]. By the 1990s, months and thousands of square kilometres in the past 30 years, polynya prevalence had reached a point at which further increase with most of the increase in season occurring in the western Ross would not affect the penguins, and the slow population decrease in Sea slope area, i.e. what is known as the Ross Passage Polynya (cf. the 1990s could be related to recovery of the minke whale [44], [45]). This trend, owing to increasing winds associated with population from whaling in the 1970 and early 1980s (see the AAO switch, is projected to continue over the next few decades Introduction: reason for the 1970s–80s increase in penguins). The [9], [11], [44]. At the same time, the latent-heat, wind-driven fact that the penguin decrease did not reach the low levels polynyas of the Ross Sea have become more persistent, i.e. their exhibited before the whaling we ascribe to climate effects and, sea-ice season is decreasing [46], which facilitates penguin foraging Figure 2. Time-series plots of the logged Ade´lie penguin colony counts at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica from 1981 to 2012. The linear regression trend lines are for the period 1981–2000. doi:10.1371/journal.pone.0091188.g002 PLOS ONE | www.plosone.org 6 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends [48], [49]). Consuming silverfish is key to large size and maximum Table 3. Summary of linear trend models for northern body condition of Ross Island penguin chicks, and thus eventual Victoria Land colony counts (log -transformed) for the years post-fledging survival (Whitehead et al. unpubl. data). Such a 1981–2000. change in survival could explain the population increase, a subject currently being explored (Dugger et al., unpubl. data). Trend/slope estimate Colony (SE est.) p-value Trends in the Northern Victoria Land Population: More Physics Franklin Island West 0.0461 (0.01009) 0.020 It is unfortunate that colony assessment became so sparse for Inexpressible Island 20.0113 (0.02224) 0.647 northern Victoria Land after 2000. Before then, trends appear to Terra Nova Bay 20.0400 (0.00897) 0.011 be approximately similar to the southern colonies. Since then, it is Wood Bay 20.0023 (0.02478) 0.932 impossible to judge trends, and it appears that the slow movement Coulman Island South 20.0361 (0.02113) 0.186 of the B-15, C-16 and C-19 icebergs along the Victoria Land coast negatively affected the northern colonies, coincidently in most of Cape Hallett 20.0137 (0.01851) 0.478 the years when counts were done. The mega-iceberg C-19 delayed Cape Cotter 0.0028 (0.04761) 0.955 sea-ice breakout offshore of most of the northern Victoria Land Values in bold text indicate statistical significance of the estimated slope colonies as it made its way north in Spring 2002. This would help parameter (r = per capita annual growth rates) at P,0.05. to explain the low counts that year, with the ice having retarded or doi:10.1371/journal.pone.0091188.t003 discouraged penguin arrival in time for egg laying (and counting). Similarly, B-15J (the largest piece remaining from B-15A, after it namely, increasing persistence of coastal polynyas that favoured broke up further) and C-16 appear to have blocked the exit of sea colony growth. ice offshore of northern colonies as they made their way north in If the earlier study by Wilson et al. [25] (2001) is correct– 2006 (another year of low counts). It would have been interesting decreases in colonies happen following years of extensive sea ice in to have had colony counts from Possession, Sven Foyn and Cape the Ross Sector–then Ade´lie penguin numbers in the Ross Sea Adare colonies in 2005, as the largest part of B-15 spent several should be decreasing (cf. in accord with increasing ice extent and summer months offshore of those colonies in late 2005 [50] (it season [44]). The obvious question is why is this not happening? passed by the more southerly Victoria Land colonies well before We propose that the large increases observed in the southern penguins would have been undertaking their spring migration and population over the last decade, as with the whales earlier, might arrival at colonies and so likely had no effect then). The effect on be the result of competitive release. Owing to the recent packing the sea ice against the coast by one small, B-15A, piece off disappearance of another trophic competitor in the southern Ross Cape Hallett in 2005 can be seen in fig. 4 in Lyver et al. [51], Sea, adult and subadult Antarctic toothfish (Dissostichus mawsoni) potentially resulting in alteration of the foraging area. We did not [47], we propose that an increase has occurred in a principal prey have a colony count that year, and the low colony size in 2006, for species of both predators, Antarctic silverfish (Pleuragramma whatever reason, seems to have been temporary. Indeed, a report antarcticum). Over the southern shelf, Antarctic silverfish are a based on an aerial survey in 2009 to revise the Cape Hallett major prey of both Ade´lie penguins and Antarctic toothfish (cf. Management Plan indicated that breeding pairs were far more Figure 3. Time series plots of the logged Ade´lie penguin breeding pair counts from colonies that were surveyed more than five times between the years 1981 and 2012 along the Victoria Land coast, Antarctica. The linear regression trend lines are for the period 1981–2000 (in accord with Fig. 2), after which counts became too infrequent to fit a regression. doi:10.1371/journal.pone.0091188.g003 PLOS ONE | www.plosone.org 7 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Figure 4. Annual colony growth rate against colony size at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica between 1981 and 2012. A fitted linear trend is indicated by the dashed lines (fitted using ordinary least squares regression). doi:10.1371/journal.pone.0091188.g004 numerous than when we did our last survey in 2006 [52]. Using a Conclusion combination of oblique photographs from an aircraft flying just As a sea-ice obligate, the Ade´lie penguin generally exists in areas outside colony boundaries and ground-truthing, the surveyors of intermediate sea-ice concentration (,15% is ideal [53]), where estimated ,64,000 breeding pairs, or a 2K-fold difference from there is adequate ice for resting but not so much that individuals the numbers counted in 2006. We cannot explain the difference. incur additional energetic cost associated with walking great However, lessons learned at Ross Island, and especially Cape distances to access open water [12], [54]. We saw the effects of too Royds, suggest that mega-iceberg presence, including lagged much ice in the trends of both the southern and northern Victoria effects (Dugger et al. unpubl. data), could well apply. Land colonies, especially with the mega-iceberg natural experi- ments. Another experiment is taking place elsewhere in Antarctica, Figure 5. Annual growth rates for Adelie penguin colonies at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica from 1981 to 2012. doi:10.1371/journal.pone.0091188.g005 PLOS ONE | www.plosone.org 8 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends as sea ice disappears and so have Ade´lie penguins [15], [16], [55], Acknowledgments [56]. On the basis of that information, predictions related to Logistics were provided by Antarctica New Zealand, with support from the changes in Ade´lie penguin populations, size and distribution, as a New Zealand Defense Force, and the US Antarctic Program. We thank the function of sea-ice presence and persistence, indicate that 75% of members of the New Zealand Antarctic Fisheries Working Group, in Ade´lie penguin colonies (70% of the breeding population) north of particular Ben Sharp and Matt Pinkerton, Cissy Pan, Christine Bezar and 70u S will decrease or disappear by 2050 owing to the the two anonymous reviewers for their reviews and contributions to this paper. disappearance of sea ice but colonies may grow or be founded at high latitude where sea ice is loosening [9]. All of the Ross Sea colonies reported in the present study, however, are situated south Author Contributions of 70u S, and may well be the last to benefit from sea-ice presence Conceived and designed the experiments: PO’BL KJB PRW. Performed if current climate trends continue. the experiments: PO’BL KJB DA AP SG GB PRW. Analyzed the data: PO’BL MB DA. Contributed reagents/materials/analysis tools: SM. Wrote the paper: PO’BL MB DA GB. References 1. 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(2003) Spatial and Science 328: 1520–1523. doi: 10.1126/science.1185779 temporal variation of diet within a presumed metapopulation of Ade´lie PLOS ONE | www.plosone.org 10 March 2014 | Volume 9 | Issue 3 | e91188 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLoS ONE Pubmed Central

Trends in the Breeding Population of Adélie Penguins in the Ross Sea, 1981–2012: A Coincidence of Climate and Resource Extraction Effects

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Abstract

Measurements of the size of Ade´lie penguin (Pygoscelis adeliae) colonies of the southern Ross Sea are among the longest biologic time series in the Antarctic. We present an assessment of recent annual variation and trends in abundance and growth rates of these colonies, adding to the published record not updated for more than two decades. High angle oblique aerial photographic surveys of colonies were acquired and penguins counted for the breeding seasons 1981–2012. In the last four years the numbers of Ade´lie penguins in the Ross and Beaufort Island colonies (southern Ross Sea metapopulation) reached their highest levels since aerial counts began in 1981. Results indicated that 855,625 pairs of Ade´lie penguins established breeding territories in the western Ross Sea, with just over a quarter (28%) of those in the southern portion, constituting a semi-isolated metapopulation (three colonies on Ross Island, one on nearby Beaufort Island). The southern population had a negative per capita growth rate of 20.019 during 1981–2000, followed by a positive per capita growth rate of 0.067 for 2001–2012. Colony growth rates for this metapopulation showed striking synchrony through time, indicating that large-scale factors influenced their annual growth. In contrast to the increased colony sizes in the southern population, the patterns of change among colonies of the northern Ross Sea were difficult to characterize. Trends were similar to southern colonies until the mid-1990s, after which the signal was lost owing to significantly reduced frequency of surveys. Both climate factors and recovery of whale populations likely played roles in the trends among southern colonies until 2000, after which depletion of another trophic competitor, the Antarctic toothfish (Dissostichus mawsoni), may explain the sharp increasing trend evident since then. Citation: Lyver PO, Barron M, Barton KJ, Ainley DG, Pollard A, et al. (2014) Trends in the Breeding Population of Ade´lie Penguins in the Ross Sea, 1981–2012: A Coincidence of Climate and Resource Extraction Effects. PLoS ONE 9(3): e91188. doi:10.1371/journal.pone.0091188 Editor: Hans-Ulrich Peter, Institute of Ecology, Germany Received November 1, 2013; Accepted February 10, 2014; Published March 12, 2014 Copyright:  2014 Lyver 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: This work was primarily funded by New Zealand’s Foundation for Research, Science and Technology grants (C09527; C09X0510) and Ministry of Science and Innovation project (C01X1001; CONT-21216-BKBN). Funding for DA, AP, and GB came from the National Science Foundation (OPP 0944411). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: Two co-authors work for commercial companies, H. T. Harvey & Associates Ecological Consultants and Bartonk Solutions. This does not alter the authors’ adherence to all the PLOS ONE policies on sharing data and materials. * E-mail: lyverp@landcareresearch.co.nz Annular Mode), are expressed through the physical environment. Introduction Examples include changes in sea-ice conditions such as concen- The underlying factors most likely to limit the abundance of tration, extent and thickness, air temperatures, winds, sea surface breeding seabirds in a region are prey or nesting space availability temperatures (SST) and precipitation (see Ainley et al. [3] and [1]. These effects are manifest in key demographic rates such as references therein). In the case of high latitude Antarctic penguins, age-specific survival, dispersal and proportion breeding. This is the issue is related to a sea-ice optimum lying between extremes especially so for central-place foragers like Antarctica’s ‘‘true’’ that can affect them in different ways [4] (see also Jenouvrier [5] pack-ice penguins, Emperor (Aptenodytes forsteri) and Ade´lie for a general application of climate optima to avian trends), as (Pygoscelis adeliae) penguins, which breed gregariously in large indicated empirically within the palaeoecological and ecological colonies [2]. The inability of these penguins to forage across vast records of Emperor and Ade´lie penguin populations [6], [7], [8], distances means that they are influenced to a greater degree than [9], [10]. A switch of the AAO in the mid-1970s from variable, volant species (e.g. albatrosses Diomedea spp.) by the local habitat negative-to-positive on a decadal scale, to almost always positive and resources and by changes in conditions and prey stocks. thereafter brought changes in winds and sea ice [11] and in turn Population responses of penguins to changing ecosystems can be affected pack-ice penguin populations [3], [6], [7]. complex. Spatio-temporal variation in climatic variables resulting Climate change, however, by no means is the total story. from phenomena such as long-term climate change, or shorter- Significant changes in Ade´lie penguin numbers could warn of term decadal atmospheric variation, i.e. factors related to the changes in the abundance of their prey and/or structure and Southern Oscillation and Antarctic Oscillation (AAO, or Southern function of the marine ecosystem owing to other factors [12]. PLOS ONE | www.plosone.org 1 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Depletion of whales and demersal fish has been associated with nests, though some expressed nervousness (a portion waving their flippers, P. Wilson pers. obs.; Brian Karl pers. obs.). Prior to 2006, large-scale changes in abundance of Antarctic penguins and other diving species, i.e. seals (Mirounga, Arctocephalus) and shags photographs were taken with a Pentax 645 medium format black and white film-back camera. This unit was upgraded in 2006 to a (Phalacrocorax spp.) [13], [14], [15], [16], [17]. In the Ross Sea, the dramatic increase in Ade´lie penguin numbers from the mid- Hassleblad H1D 22 MP medium-format digital camera, which was then replaced with a Canon EOS 1DS Mark III camera for 1970s to the early 1980s, followed by slow decline, has been correlated with the depletion by commercial whaling and then the 2011/12 season. We used photographs that were taken each year as close as recovery of Antarctic minke whales (Balaenoptera bonaerensis)in International Whaling Commission Areas V and VI [18], [19]. possible to 1 December (range of dates: 25 November to 8 December) each season. This is a date on which the colony Ross Sea penguins and minke whales feed on the same prey [20] and the penguins have since been found to begin their wintering population, owing to its seasonal dynamics, was represented almost entirely by one member of each penguin pair incubating its mode in the area where most of this whaling occurred: waters eggs, and minimal numbers of non-breeders [12]. Even though north of Victoria Land [21]. our surveys were conducted within a two week window, it is Reliable repeated assessments over the long term are therefore possible that phenology, monitored on the ground at Ross Island crucial for understanding how these and other factors influence colonies, still accounts for a small proportion of the inter-annual breeding population sizes and dynamics for high latitude penguins, variation we observed. Census data from surveys conducted prior and hence for informing management. The Ade´lie penguin is one to 1981 were not used because they were ground-based and only of the species monitored by the Commission for the Conservation for two of the three colonies – Cape Royds and Cape Bird. The of Antarctic Marine Living Resources (CCAMLR) as part of its population data from the years 1998–2012 are presented here for CCAMLR Ecosystem Monitoring Program (CEMP) to potentially the first time. For a full description of survey methods (e.g. detect anthropogenic effects on Antarctic marine ecosystems [22]. prioritization, location and flight approaches for colonies, and In the Ross Sea sector of the Southern Ocean, Ade´lie penguins camera specifications) please refer to references [22], [24] and breed over a latitudinal range of 1200 km, from the Balleny [25]. Operational permits were approved and issued by New Islands (Buckle Island, 66u 509 S) north of the Ross Sea to Ross Zealand’s Ministry of Foreign Affairs and Trade under the Island (Cape Royds, 77u 339 S) in the south (Fig. 1) and therefore Antarctic (Environmental Protection) Act 1994 and Landcare may be exposed to a range of environmental conditions and Research’s Animal Ethics Committee 2005 and 2010 respectively habitats, e.g. abyssal ocean, continental slope and shelf ecosystems. (0509/01 and 10/09/01). Data is available upon request via: The objective of this study, therefore, was to add to the long-term http://www.landcareresearch.co.nz/resources/data/adelie-census- record and measure variation in the size of the Ade´lie penguin data). breeding populations in subregions of the western Ross Sea during the period 1981–2012. Owing to the infrequent surveys along the Manual and Semi-automated Mapping and Counting of northern Victoria Land coast after the mid-1990s, we focused our assessment primarily on the annual or near-annual surveys of the Colonies southernmost cluster (and likely metapopulation; see [23]) of Prior to 2006, film negatives were developed in a dark room, Ade´lie penguin colonies: three colonies on Ross Island [Cape and the resulting photographs of the colony were printed and manually joined together. Once a mosaic of the colony was Royds, Cape Bird (North, Middle and South), Cape Crozier (East and West)] and one on Beaufort Island, about 20 km north of constructed, the appropriate photographs were enlarged and each territory occupied by a penguin counted by marking it with a dot Cape Bird. We examined a range of diagnostics such as means and variations in colony size, rates of change in abundance with time to ensure that each was counted only once. This method of counting was slow, and it was difficult to verify counts at a later (annual growth rates), and evidence of trends and cycles. To conclude we offer hypotheses that might explain the trends and stage. However, the method had the benefit that a physical record was kept for each census. changes in colony sizes observed over the past three decades. From 2006, the colony images were captured digitally but the photographs were still processed and penguins counted manually. Methods In 2010, semi-automatic penguin counting software was developed Census Surveys of Colonies so that colony mapping, counts and verification of counts could occur on the computer screen [26]. High angle oblique aerial photographs of Ade´lie penguin adults occupying nesting territories at colonies along the Victoria Land coast and offshore islands were acquired for the period 1981–2012 Time-Series Analysis (see Taylor and Wilson [24](1990) and Wilson et al. [25] (2001) for The Cape Bird totals are the sum of counts of 3 partitions of the discussion of trends from 1959 to 1997, based on both aerial and colony and the Cape Crozier counts are the sum of 2 partitions of ground counts, as well as the discovery of 11 previously unreported that colony, but in 3 different years counts from one of the three breeding colonies). We define ‘‘nesting territories’’ as sites Cape Bird partitions were not available. To avoid biasing the total occupied and defended by both breeding and non-breeding adults colony count towards zero these missing values for Cape Bird were (see below). Colonies on Ross Island (Cape Royds, Cape Bird and interpolated by fitting a cubic smoothing spline to the colony Cape Crozier) and Beaufort Island (Fig. 1 – herein referred to as partition time series using the ‘‘zoo’’ package in the statistical the southern metapopulation) were photographed annually from a software ‘‘R’’ [27]. Variation in counts within a colony was helicopter flying at an altitude of 2000–2500 feet (610–765 m) assessed by calculating the standard deviation of the logarithmic above ground level. Colonies along the northern Victoria Land transformation of the counts (s) [28]. coast (Fig. 1) were photographed only occasionally after the mid- Visual inspection of the colony time series indicated a potential 1990s, from the open paratroop doors of a C-130 Hercules flying change point in the trends in counts of southern colonies around at a minimum altitude of 2,500 feet a.g.l. Observations from the the years 2000–2001. To assess differences in trends 1981–2000 vs ground showed that over-flights of helicopters and C-130 aircraft 2001–2012, a generalized least squares model was fitted to each of at altitudes of at least 2000 feet a.g.l. did not force birds to leave the log -transformed Ross Island colony counts with first-order PLOS ONE | www.plosone.org 2 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Figure 1. Distribution and size categories (based on 1981–2012 means) of Ade´lie penguin colonies from the western Ross Sea, Antarctica. doi:10.1371/journal.pone.0091188.g001 correlation (AR(1)) in the error term to account for the inherent the confidence intervals of the mean correlation coefficient were dependence of a count in one year on the count last year. Two estimated using the bootstrap algorithm of Bjørnstad et al. [30] models were fitted for each colony, one with a linear trend with (1999), implemented in the ‘‘ncf’’ package for the statistical time across all years (1981–2012), and one with different linear software ‘‘R’’. trends in the periods 1981–2000 and 2001–2012, in which the two periods were specified using dummy variables. The best fitting Results model out of the two was selected using the Akaike Information Size and Variation in Breeding Pairs of Ade´lie Penguin Criteria corrected for small sample sizes (AICc). Phase plots of current colony counts against lagged counts (t-1 vs Colonies in the Ross Sea t; both log -transformed) were constructed as a visual means of During our 30-year survey period 855,625 pairs of Ade´lie assessing density dependence [32]. To identify any periodicities or penguins on average held nesting territories just prior to hatching density dependence (Year 1 to Year 10) in the time series of colony at colonies in the western Ross Sea (Table 1). Around a quarter counts, autocorrelation functions (ACF) and partial rate correla- (28%) of this number breed as part of the southern metapopulation tion functions (PRCF) were estimated for each of the three Ross with two-thirds (64%) of those birds concentrated at Cape Crozier Island colonies [29]. The significance of the correlations was tested (Table 1). The variation (or amplitude, s-value) in annual colony with Bartlett’s band 6 2/!n, where n is the length of time series. size variations across colonies in this population was similar Spatio-temporal synchrony between annual colony growth rates (range = 0.11 to 0.15; Table 1). The s-values indicate that the (r = log (N ) – log (N )) was assessed by calculating cross- average ‘‘peak to trough’’ ratio of counts is around one-third to t e t+1 e t correlation coefficients (r ) between all pairs of the Ross and one-half an order of magnitude (s = 0.35 is equivalent to one order i,j Beaufort island colonies. The mean correlation coefficient was of magnitude variation) indicating a lack of cycles in the data [27]. calculated to quantify spatial synchrony across colonies in the Counts of Ade´lie penguin breeding pairs in the northern Victoria southern metapopulation. Because of autocorrelation in the data, Land population over the last 20 years have been infrequent so the PLOS ONE | www.plosone.org 3 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends variation, although also quite similar across colonies (range = 0.09 Discussion to 0.22; Table 1), needs to be interpreted with caution. Status and Trends in the Ross Sea Ade´lie Penguin Population Trends in Size of Ade´lie Penguin Colonies in the Ross Sea A regression model with two separate trend lines fitted the The aerial survey data reported here provide the most recent counts of Ade´lie penguin breeding pairs in the Ross Sea, extending colony count data best for the Beaufort Island, Cape Bird and Cape Crozier colonies, but not for Cape Royds, where a single in time by 2.5 decades one of the longest monitored Antarctic penguin populations. In the last four years, the numbers of Ade´lie trend line was selected (Table 2). Our model indicated a generally decreasing trend in the number of breeding pairs at the Beaufort penguins, at least in the southern Ross Sea, have grown to their highest levels since aerial counts began (1981), as well as since all Island, Cape Bird and Cape Crozier colonies between 1981 and 2000, then an increasing trend from 2001 to 2012 (Table 2; Fig. 2). counts began in 1959 (cf. [23]). Even so, our mean count of 855,625 breeding pairs for the Ross Sea was still lower than the The small Royds colony appeared to be stable until it decreased sharply in 2000 and 2001, followed by a period of no growth or mean count of 938,877 breeding pairs reported by R.H. Taylor during the 1980s (pers. comm. in Woehler [31] 1993). This slight growth beginning in the last two years. In aggregate, this difference can be potentially explained by the infrequent surveys of metapopulation had an average negative per capita annual growth rate of 20.019 over the 1981–2000 period followed by an average Victoria Land colonies, where in the past approximately 75% of the Ross Sea population have bred, over the last 25 years when positive per capita annual growth rate of 0.067 over the 2001– 2012 period, reflecting primarily the pattern in the larger colonies numbers were potentially substantially lower than in the 1980s. We do not report numbers from the four Victoria Land colonies (not Royds). The two larger colonies had close to twice (1.8 times) the number of birds in 2012, than the 30-year average (Table 1). west of Cape Adare (Fig. 1) (no more than ,3,000 pairs [12], Lyver unpubl. data). There was synchrony between colonies in annual changes in size through this period with a common low point in counts around The most current assemblage of counts indicates about 38% of Year 2001 for all colonies (Fig. 2). the circum-Antarctic Ade´lie penguin population breeds in the Changes in abundance of Ade´lie penguins at seven colonies of Ross Sea [12]. Coupled with observed increases in the Ross Sea northern Victoria Land for which we had data from six or more over the last decade, expanding distributions in east Antarctica surveys over the 30 years were variable. There appeared to be [32], and decreases in colonies in the northern Antarctic Peninsula initial stability or perhaps decrease through 1991, but thereafter, region but increases in the south [16], this percentage may still be with sparse counts, no clear trend was evident (Table 3; Fig. 3). approximately correct. A large concentration (historically ,47% of the Ross Sea population) in the extreme northern Victoria Land focuses around four colonies: Possession Island, Foyn Island, Colony Size Regulation Downshire Cliffs, and Cape Adare (Fig. 1). We have limited The auto-correlation functions (ACF) for log -transformed information about recent trends in these colonies, although some colony sizes showed no evidence of cycles in the time series, with of them might be space-limited. It is likely that these large significant lags occurring only at 1 year or both years 1 and 2, concentrations occur where they do because of nesting habitat though the length of the time series is relatively short for such availability, proximity to persistent polynyas where open water detection. The slow decay of the ACF to negative values at high facilitates access to prey [12], and proximity to the highly lags is indicative of a trend in the data (as discussed in the previous productive Ross Sea Slope Front [33]. section). The partial rate correlation functions (PRCF) for the rates The presence of unoccupied sub-colony mounds with ample of change versus log -transformed colony size all showed a supplies of pebbles for nest-building indicates that the colonies on significant negative correlation at lag 1 indicative of direct density Ross Island are not space-limited. However, recent recession of ice dependence in the number of pairs returning to the colony each fields on Beaufort Island have resulted in more nesting habitat, year. This indicates that high colony counts in one year tend to meaning that recruits within this metapopulation no longer have result in lower growth rates to the following year, and vice versa: to emigrate to the Ross Island colonies to find nesting space [23]. low colony counts in one year tend to result in higher growth rates Therefore, only recently has Beaufort been able to grow. We to the following year (Fig. 4). There were also significant negative suggest that the numbers breeding in the southern colonies are correlations between rates of change and colony size 8 years now more likely to be limited by food accessibility, mediated in previously for Cape Royds and Cape Crozier. Phase plots for Cape Royds and Cape Crozier showed relatively small back-and- part by environmental stochasticity (especially fast ice cover) in the case of Cape Royds and perhaps Cape Bird [34] and by inter- and forth fluctuations about the mean colony size throughout the intra-specific competition at Cape Crozier and Beaufort Island 1980s and 1990s, indicative of direct density dependence, followed [20], [23], [35]. by larger variation in colony sizes from the Year 2000 on, indicating looser regulation. The phase plot for Cape Bird showed consistent clockwise orbits, indicative of ongoing delayed density- ´ Drivers of Adelie Penguin Abundance in the Ross Sea dependent feedback on colony size. The similar low level of amplitude associated with colony size variation across the southern metapopulation indicates that Synchrony in Annual Colony Growth Rates colonies could be responding in concert to a single or multiple Annual colony growth rates (r) for the southern population common drivers (except for Royds during and after the mega- showed a striking level of synchrony through time (Fig. 5). This iceberg B-15 era; see below). This is supported by the high level of was confirmed by a high mean (cross-) correlation for the Ross and synchrony and correlation in annual growth (Fig. 5). The relationship between annual colony growth rates and size indicates Beaufort island colonies of 0.59, with a 95% (bootstrapped) confidence interval of 0.35–0.77. The lowest levels of synchrony that a form of density dependence could be influencing colonies, supported by the fact that initially recent growth at Beaufort was were between Beaufort Island and the other colonies (R = 0.35– 0.59). Synchrony between the other three colonies (Cape Royds, due to infilling of the colony followed by expansion into new Cape Bird and Cape Crozier) was higher, with correlation breeding habitat [33]. Since currently there is ample space for coefficients of 0.68–0.77. additional growth at all these colonies (see [23]), competition for PLOS ONE | www.plosone.org 4 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Table 1. Mean colony counts of nesting territories (with colony counts from Ross Island 2012 for comparison) and s, a measure of the amplitude of colony size variations (n is the total number of counts per colony), for colonies in the southern Ross Sea metapopulation and along the Victoria Land coast between 1981 and 2012. Colony Mean colony count (Colony counts 2012) sN n contiguous Ross Island metapopulation Cape Royds 2,825 (3083) 0.11 30 30 Cape Bird 43,321 (75,696) 0.13 30 30 Cape Crozier 153,632 (272,340) 0.15 28 28 Beaufort Island 39,391 0.13 17 9 Victoria Land Franklin Island West 60,540 0.11 7 2 Franklin Island East 1,110 0.12 8 2 Inexpressible Island 24,450 0.09 9 2 Terra Nova Bay 11,234 0.13 9 2 Wood Bay 1,890 0.13 8 2 Cape Anne 268 0.22 6 1 Coulman Island South 17,991 0.09 6 4 Coulman Island Middle 4,325 0.11 9 5 Coulman Island North 1,694 0.10 8 4 Cape Jones 153 0.14 6 2 Mandible Cirque 16,837 0.10 3 2 Cape Phillips 3,921 0.08 4 3 Cape Wheatstone 2,746 0.18 6 3 Cape Cotter 38,252 0.16 8 3 Cape Hallett 42,628 0.14 14 8 Foyn Island 30,494 0.12 6 1 Possession Island 111,306 0.15 3 1 Downshire Cliffs 19,617 0.12 5 2 Cape Adare 227,000 0.09 4 1 doi:10.1371/journal.pone.0091188.t001 food or food availability is the most likely variable affecting birds’ remaining in place in McMurdo Sound for most of the period body condition and subsequent survival or decision whether to 2001–2005; besides nest desertions, many adults eventually return to breed in the following year. emigrated to Cape Bird [40]. Thus, recovery of the Cape Royds colony has been slow, showing positive signs only in the last couple of years. In contrast, the colonies at Beaufort, Bird and Crozier, Effects of Physical Changes in the Penguins’ Environment which were less affected by the increased sea ice, except in the Among the possible common drivers is sea-ice variation, with initial iceberg year, subsequently grew throughout the remaining the mega-icebergs showing this quite well at the local, mesoscale. mega-iceberg era up to the present. The depression in abundance of Ade´lie penguins in the southern The effects of ice bergs and the altered sea-ice regime were not Ross Sea population in 2001 was a common low point coinciding confined just to the southern Ade´lie penguins. B-15A and C-16 with the arrival of the giant icebergs B-15A and C-16 in January presence resulted in an initial decrease in Beaufort Island and 2001, and which remained in place until winter 2005. These Cape Crozier emperor penguins, followed by slow recoveries still icebergs, as well as B-15B, resulted in a one-season reduction in ongoing [41], [42] (Ballard et al. unpubl. data). The extensive fast primary production in the Ross Sea polynya, 2000/01 [36], [37], ice that remained in McMurdo Sound 2001–2005 resulted in a as well as an alteration of surface circulation [38]. The calving of depression in Weddell seal (Leptonychotes weddelli) numbers, but an even larger iceberg in 2002/03, C-19, also led to a one-season which recovered entirely once the icebergs departed and annual decrease in production (owing to more sea ice, and less ocean fast ice returned [43]. exposed to sunlight; [39], C. Smith, unpubl. data). While grounded, B-15A and C-16 prevented the wind from blowing Sea-ice cover at the larger scale can also affect Ade´lie penguins in a number of ways. A previous study analysing trends up to 1998 sea ice from the southwestern Ross Sea northward, except in 2003 when winds were particularly strong. Lots of sea ice decreased demonstrated a correlation between declines in the southern access to the ocean and food [4], [9]. colonies 4–5 years after anomalously extensive sea ice in the Ross Many Ade´lie penguin adults failed or abandoned breeding Sea sector of the Southern Ocean [25]. Those authors hypoth- attempts early in the breeding season in the initial year of the B- esized that juvenile Ade´lie penguin survivorship decreased in years 15A and C-16 iceberg groundings (2001/02). In the case of Cape when extensive sea ice carried the penguins well beyond the Royds, conditions were especially daunting with 70 km of fast ice productive feeding grounds that lie south of the Southern PLOS ONE | www.plosone.org 5 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Table 2. Summary of trend models for Cape Royds, Cape Bird and Cape Crozier (Ross Island) and Beaufort Island colony counts (log -transformed) with predictor units in years from 1981 to 2012. Best model (1 or 2 Trend 1981–2000 slope estimate Trend 2001–2012 slope estimate Colony linear trends) (std error estimate) (std error estimate) Cape Royds 1 20.0085 (0.00797) Cape Bird 2 20.0245 (0.00862) 0.0755 (0.01523) Cape Crozier 2 20.0223 (0.00784) 0.0981 (0.01213) Beaufort Island 2 20.0214 (0.01357) 0.1028 (0.03318) Values in bold text indicate statistical significance of the estimated slope parameter (r = per capita annual growth rates) at P,0.05. doi:10.1371/journal.pone.0091188.t002 Boundary of the Antarctic Circumpolar Current (SBACC). If the during the breeding season at least to a point, after which further winter-sea-ice extent in the Ross Sea sector regularly extended polynya growth is neutral to penguin well-being. beyond the SBACC then natural growth rates of Ade´lie penguin colonies could be affected, given that sea-ice extent has been Effects of Biological Changes in the Penguins’ growing in the Ross Sea sector, including more years of ice Environment extending north of the SBACC [44]). The sea-ice season and The more favorable polynya behaviour also likely played a large-scale extent in the Ross Sea region has increased by 3 complex role in trends through the 1990s [3]. By the 1990s, months and thousands of square kilometres in the past 30 years, polynya prevalence had reached a point at which further increase with most of the increase in season occurring in the western Ross would not affect the penguins, and the slow population decrease in Sea slope area, i.e. what is known as the Ross Passage Polynya (cf. the 1990s could be related to recovery of the minke whale [44], [45]). This trend, owing to increasing winds associated with population from whaling in the 1970 and early 1980s (see the AAO switch, is projected to continue over the next few decades Introduction: reason for the 1970s–80s increase in penguins). The [9], [11], [44]. At the same time, the latent-heat, wind-driven fact that the penguin decrease did not reach the low levels polynyas of the Ross Sea have become more persistent, i.e. their exhibited before the whaling we ascribe to climate effects and, sea-ice season is decreasing [46], which facilitates penguin foraging Figure 2. Time-series plots of the logged Ade´lie penguin colony counts at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica from 1981 to 2012. The linear regression trend lines are for the period 1981–2000. doi:10.1371/journal.pone.0091188.g002 PLOS ONE | www.plosone.org 6 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends [48], [49]). Consuming silverfish is key to large size and maximum Table 3. Summary of linear trend models for northern body condition of Ross Island penguin chicks, and thus eventual Victoria Land colony counts (log -transformed) for the years post-fledging survival (Whitehead et al. unpubl. data). Such a 1981–2000. change in survival could explain the population increase, a subject currently being explored (Dugger et al., unpubl. data). Trend/slope estimate Colony (SE est.) p-value Trends in the Northern Victoria Land Population: More Physics Franklin Island West 0.0461 (0.01009) 0.020 It is unfortunate that colony assessment became so sparse for Inexpressible Island 20.0113 (0.02224) 0.647 northern Victoria Land after 2000. Before then, trends appear to Terra Nova Bay 20.0400 (0.00897) 0.011 be approximately similar to the southern colonies. Since then, it is Wood Bay 20.0023 (0.02478) 0.932 impossible to judge trends, and it appears that the slow movement Coulman Island South 20.0361 (0.02113) 0.186 of the B-15, C-16 and C-19 icebergs along the Victoria Land coast negatively affected the northern colonies, coincidently in most of Cape Hallett 20.0137 (0.01851) 0.478 the years when counts were done. The mega-iceberg C-19 delayed Cape Cotter 0.0028 (0.04761) 0.955 sea-ice breakout offshore of most of the northern Victoria Land Values in bold text indicate statistical significance of the estimated slope colonies as it made its way north in Spring 2002. This would help parameter (r = per capita annual growth rates) at P,0.05. to explain the low counts that year, with the ice having retarded or doi:10.1371/journal.pone.0091188.t003 discouraged penguin arrival in time for egg laying (and counting). Similarly, B-15J (the largest piece remaining from B-15A, after it namely, increasing persistence of coastal polynyas that favoured broke up further) and C-16 appear to have blocked the exit of sea colony growth. ice offshore of northern colonies as they made their way north in If the earlier study by Wilson et al. [25] (2001) is correct– 2006 (another year of low counts). It would have been interesting decreases in colonies happen following years of extensive sea ice in to have had colony counts from Possession, Sven Foyn and Cape the Ross Sector–then Ade´lie penguin numbers in the Ross Sea Adare colonies in 2005, as the largest part of B-15 spent several should be decreasing (cf. in accord with increasing ice extent and summer months offshore of those colonies in late 2005 [50] (it season [44]). The obvious question is why is this not happening? passed by the more southerly Victoria Land colonies well before We propose that the large increases observed in the southern penguins would have been undertaking their spring migration and population over the last decade, as with the whales earlier, might arrival at colonies and so likely had no effect then). The effect on be the result of competitive release. Owing to the recent packing the sea ice against the coast by one small, B-15A, piece off disappearance of another trophic competitor in the southern Ross Cape Hallett in 2005 can be seen in fig. 4 in Lyver et al. [51], Sea, adult and subadult Antarctic toothfish (Dissostichus mawsoni) potentially resulting in alteration of the foraging area. We did not [47], we propose that an increase has occurred in a principal prey have a colony count that year, and the low colony size in 2006, for species of both predators, Antarctic silverfish (Pleuragramma whatever reason, seems to have been temporary. Indeed, a report antarcticum). Over the southern shelf, Antarctic silverfish are a based on an aerial survey in 2009 to revise the Cape Hallett major prey of both Ade´lie penguins and Antarctic toothfish (cf. Management Plan indicated that breeding pairs were far more Figure 3. Time series plots of the logged Ade´lie penguin breeding pair counts from colonies that were surveyed more than five times between the years 1981 and 2012 along the Victoria Land coast, Antarctica. The linear regression trend lines are for the period 1981–2000 (in accord with Fig. 2), after which counts became too infrequent to fit a regression. doi:10.1371/journal.pone.0091188.g003 PLOS ONE | www.plosone.org 7 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends Figure 4. Annual colony growth rate against colony size at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica between 1981 and 2012. A fitted linear trend is indicated by the dashed lines (fitted using ordinary least squares regression). doi:10.1371/journal.pone.0091188.g004 numerous than when we did our last survey in 2006 [52]. Using a Conclusion combination of oblique photographs from an aircraft flying just As a sea-ice obligate, the Ade´lie penguin generally exists in areas outside colony boundaries and ground-truthing, the surveyors of intermediate sea-ice concentration (,15% is ideal [53]), where estimated ,64,000 breeding pairs, or a 2K-fold difference from there is adequate ice for resting but not so much that individuals the numbers counted in 2006. We cannot explain the difference. incur additional energetic cost associated with walking great However, lessons learned at Ross Island, and especially Cape distances to access open water [12], [54]. We saw the effects of too Royds, suggest that mega-iceberg presence, including lagged much ice in the trends of both the southern and northern Victoria effects (Dugger et al. unpubl. data), could well apply. Land colonies, especially with the mega-iceberg natural experi- ments. Another experiment is taking place elsewhere in Antarctica, Figure 5. Annual growth rates for Adelie penguin colonies at Cape Royds, Cape Bird, Cape Crozier and Beaufort Island, Antarctica from 1981 to 2012. doi:10.1371/journal.pone.0091188.g005 PLOS ONE | www.plosone.org 8 March 2014 | Volume 9 | Issue 3 | e91188 ´ Adelie Penguin Population Trends as sea ice disappears and so have Ade´lie penguins [15], [16], [55], Acknowledgments [56]. On the basis of that information, predictions related to Logistics were provided by Antarctica New Zealand, with support from the changes in Ade´lie penguin populations, size and distribution, as a New Zealand Defense Force, and the US Antarctic Program. We thank the function of sea-ice presence and persistence, indicate that 75% of members of the New Zealand Antarctic Fisheries Working Group, in Ade´lie penguin colonies (70% of the breeding population) north of particular Ben Sharp and Matt Pinkerton, Cissy Pan, Christine Bezar and 70u S will decrease or disappear by 2050 owing to the the two anonymous reviewers for their reviews and contributions to this paper. disappearance of sea ice but colonies may grow or be founded at high latitude where sea ice is loosening [9]. All of the Ross Sea colonies reported in the present study, however, are situated south Author Contributions of 70u S, and may well be the last to benefit from sea-ice presence Conceived and designed the experiments: PO’BL KJB PRW. Performed if current climate trends continue. the experiments: PO’BL KJB DA AP SG GB PRW. Analyzed the data: PO’BL MB DA. Contributed reagents/materials/analysis tools: SM. Wrote the paper: PO’BL MB DA GB. References 1. 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(2003) Spatial and Science 328: 1520–1523. doi: 10.1126/science.1185779 temporal variation of diet within a presumed metapopulation of Ade´lie PLOS ONE | www.plosone.org 10 March 2014 | Volume 9 | Issue 3 | e91188

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Published: Mar 12, 2014

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