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      Sexual and individual foraging segregation in Gentoo penguins Pygoscelis papua from the Southern Ocean during an abnormal winter

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          Abstract

          Knowledge about sexual segregation and gender-specific, or indeed individual specialization, in marine organisms has improved considerably in the past decade. In this context, we tested the “Intersexual Competition Hypothesis” for penguins by investigating the feeding ecology of Gentoo penguins during their austral winter non-breeding season. We considered this during unusual environmental conditions (i.e. the year 2009 had observations of high sea surface and air temperatures) in comparison with the long term average at Bird Island, South Georgia. Through conventional (i.e. stomach contents) and stable isotopic values from red blood cells, plasma and feathers of both male and female Gentoo penguins, we showed that there were significant differences between sexes, with males feeding mainly on fish (54% by mass) followed by crustaceans (38%) whereas females fed mainly on crustaceans (89% by mass) followed by fish (4%). Themisto gaudichaudii was the most important crustacean prey for males (64% by mass; 82% by number; 53% by frequency of occurrence) and females (63% by mass; 77% by number; 89% by frequency of occurrence), contrasting with all previous studies that found Antarctic krill Euphausia superba were generally the main prey. Stable isotopic data showed that, in terms of habitat use (based on δ 13C), there were significant differences in short-term carbon signatures between males and females (based on plasma and red blood cells), suggesting that both sexes explored different habitats, with females exploring more offshore pelagic waters and males feeding more in coastal benthic waters. Based on δ 15N, males fed on significantly higher trophic level than females (based on plasma and red blood cells), in agreement with our diet results., Thus, Gentoo penguins behave in a similar manner to other non-breeding penguins species (e.g. king, macaroni and rockhopper penguins), albeit at a smaller spatial scale (as they do not disperse as these other penguins do), in that they have a wider habitat and trophic niche during the Antarctic Winter (in comparison to Summer). We also detected individual specialization in feeding/trophic levels for each gender, with certain males feeding mainly on fish and certain females mainly on crustaceans, which may be driven the prevailing environmental conditions that lead individuals to search for alternative prey, and cause sexual diet segregation. Our results provide further information to help improve understanding about sexual segregation and individual specialization of marine organisms, while contributing valuable information on the winter diet for Antarctic monitoring programs and for modelling Antarctic marine food webs.

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          Most cited references103

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          Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material.

          Procedures utilizing Chelex 100 chelating resin have been developed for extracting DNA from forensic-type samples for use with the PCR. The procedures are simple, rapid, involve no organic solvents and do not require multiple tube transfers for most types of samples. The extraction of DNA from semen and very small bloodstains using Chelex 100 is as efficient or more efficient than using proteinase K and phenol-chloroform extraction. DNA extracted from bloodstains seems less prone to contain PCR inhibitors when prepared by this method. The Chelex method has been used with amplification and typing at the HLA DQ alpha locus to obtain the DQ alpha genotypes of many different types of samples, including whole blood, bloodstains, seminal stains, buccal swabs, hair and post-coital samples. The results of a concordance study are presented in which the DQ alpha genotypes of 84 samples prepared using Chelex or using conventional phenol-chloroform extraction are compared. The genotypes obtained using the two different extraction methods were identical for all samples tested.
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            Recent changes in phytoplankton communities associated with rapid regional climate change along the western Antarctic Peninsula.

            The climate of the western shelf of the Antarctic Peninsula (WAP) is undergoing a transition from a cold-dry polar-type climate to a warm-humid sub-Antarctic-type climate. Using three decades of satellite and field data, we document that ocean biological productivity, inferred from chlorophyll a concentration (Chl a), has significantly changed along the WAP shelf. Summertime surface Chl a (summer integrated Chl a approximately 63% of annually integrated Chl a) declined by 12% along the WAP over the past 30 years, with the largest decreases equatorward of 63 degrees S and with substantial increases in Chl a occurring farther south. The latitudinal variation in Chl a trends reflects shifting patterns of ice cover, cloud formation, and windiness affecting water-column mixing. Regional changes in phytoplankton coincide with observed changes in krill (Euphausia superba) and penguin populations.
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              Marine pelagic ecosystems: the west Antarctic Peninsula.

              The marine ecosystem of the West Antarctic Peninsula (WAP) extends from the Bellingshausen Sea to the northern tip of the peninsula and from the mostly glaciated coast across the continental shelf to the shelf break in the west. The glacially sculpted coastline along the peninsula is highly convoluted and characterized by deep embayments that are often interconnected by channels that facilitate transport of heat and nutrients into the shelf domain. The ecosystem is divided into three subregions, the continental slope, shelf and coastal regions, each with unique ocean dynamics, water mass and biological distributions. The WAP shelf lies within the Antarctic Sea Ice Zone (SIZ) and like other SIZs, the WAP system is very productive, supporting large stocks of marine mammals, birds and the Antarctic krill, Euphausia superba. Ecosystem dynamics is dominated by the seasonal and interannual variation in sea ice extent and retreat. The Antarctic Peninsula is one among the most rapidly warming regions on Earth, having experienced a 2 degrees C increase in the annual mean temperature and a 6 degrees C rise in the mean winter temperature since 1950. Delivery of heat from the Antarctic Circumpolar Current has increased significantly in the past decade, sufficient to drive to a 0.6 degrees C warming of the upper 300 m of shelf water. In the past 50 years and continuing in the twenty-first century, the warm, moist maritime climate of the northern WAP has been migrating south, displacing the once dominant cold, dry continental Antarctic climate and causing multi-level responses in the marine ecosystem. Ecosystem responses to the regional warming include increased heat transport, decreased sea ice extent and duration, local declines in icedependent Adélie penguins, increase in ice-tolerant gentoo and chinstrap penguins, alterations in phytoplankton and zooplankton community composition and changes in krill recruitment, abundance and availability to predators. The climate/ecological gradients extending along the WAP and the presence of monitoring systems, field stations and long-term research programmes make the region an invaluable observatory of climate change and marine ecosystem response.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                31 March 2017
                2017
                : 12
                : 3
                : e0174850
                Affiliations
                [1 ]Marine and Environmental Sciences Centre, Department of Life Sciences, University of Coimbra, Coimbra, Portugal
                [2 ]British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge, UK
                [3 ]Cardiff University, Cardiff School of Biosciences, Sir Martin Evans Building, Cardiff, United Kingdom
                [4 ]Royal Belgian Institute of Natural Sciences, OD Taxonomy and Phylogeny, Rue Vautier 29, Bruxelles, Belgium
                [5 ]Centre d´Etudes Biologiques de Chizé, UPR 7372 du CNRS-Université de La Rochelle, Villiers-en-Bois, France
                Evergreen State College, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: JX PT GT YC.

                • Data curation: JX.

                • Formal analysis: JX FC RM YC.

                • Funding acquisition: JX PT.

                • Investigation: JX PT FC SA DF EE RV RM CB.

                • Methodology: JX PT FC SA DF EE RV RM CB.

                • Project administration: JX PT.

                • Resources: JX PT.

                • Software: JX FC RM.

                • Supervision: JX PT YC.

                • Validation: JX.

                • Visualization: JX FC RM.

                • Writing – original draft: JX PT FC GT RM YC.

                • Writing – review & editing: JX PT FC GT SA DF EE RV RM CB YC.

                [¤]

                Current address: Graduate School of the National Oceanography Centre Southampton, University of Southampton, Waterfront Campus, European Way, Southampton, United Kingdom.

                Author information
                http://orcid.org/0000-0002-9621-6660
                Article
                PONE-D-16-23764
                10.1371/journal.pone.0174850
                5376302
                28362847
                1789966a-6614-4e14-9187-03b9c4fecd05
                © 2017 Xavier 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.

                History
                : 15 June 2016
                : 16 March 2017
                Page count
                Figures: 6, Tables: 7, Pages: 25
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001871, Fundação para a Ciência e a Tecnologia;
                Award ID: IF/00616/2013
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001871, Fundação para a Ciência e a Tecnologia;
                Award ID: SFRH/BPD/95372/2013
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001871, Fundação para a Ciência e a Tecnologia;
                Award ID: SFRH/BD/84030/2012
                Award Recipient :
                This work is part of SCAR AnT-ERA, ICED, BAS-CEPH programs. JX is supported by the Investigator FCT program (IF/00616/2013) and FRC is supported by the Foundation for Science and Technology (Portugal) and the European Social Fund (POPH, EU) through a post-doc grant (SFRH/BPD/95372/2013). RPV is currently supported by a doctoral grant from the Portuguese Science Foundation (SFRH/BD/84030/2012). This study benefited from the strategic program of MARE, financed by FCT (MARE - UID/MAR/04292/2013)”.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Animals
                Vertebrates
                Amniotes
                Birds
                Seabirds
                Penguins
                People and Places
                Geographical Locations
                Antarctica
                Biology and Life Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Medicine and Health Sciences
                Anatomy
                Body Fluids
                Blood
                Blood Plasma
                Biology and Life Sciences
                Physiology
                Body Fluids
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                Blood Plasma
                Medicine and Health Sciences
                Physiology
                Body Fluids
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                Blood Plasma
                Biology and Life Sciences
                Organisms
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                Invertebrates
                Arthropoda
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                Biology and Life Sciences
                Behavior
                Animal Behavior
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                Zoology
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                Foraging
                Biology and Life Sciences
                Organisms
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                Biology and Life Sciences
                Ecology
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                Trophic Interactions
                Ecology and Environmental Sciences
                Ecology
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                Nutrition
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                Medicine and Health Sciences
                Nutrition
                Diet
                Custom metadata
                The relevant data are included in the paper and its Supporting Information file. For further data requests, please contact the corresponding author at jccx@ 123456cantab.net .

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