Skip to main content

Advertisement

Log in

Seasonal consistency and individual variation in foraging strategies differ among and within Pygoscelis penguin species in the Antarctic Peninsula region

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Past research during the breeding season in the Antarctic Peninsula region indicates that gentoo penguins (Pygoscelis papua) are generalist foragers whereas Adélie (P. adeliae) and chinstrap (P. antarcticus) penguins tend to specialize on Antarctic krill (Euphausia superba). However, little is known about the degree of temporal consistency in the diets and foraging habitats of these three species, particularly at the individual level. Such year-round and inter-annual dietary understanding is important to help interpret contrasting trends in their populations. We used carbon and nitrogen stable isotope analysis of blood and feathers to evaluate seasonal shifts in diet and individual foraging consistency within Pygoscelis penguin species breeding in the South Shetland Islands as well as among three geographically distinct gentoo penguin populations in the western Antarctic Peninsula and South Shetland Islands. We found that gentoo penguins exhibited a generalist foraging strategy with individual consistency, Adélie penguins exhibited an intermediate generalist foraging strategy with little individual consistency, and chinstrap penguins exhibited a specialized diet with little inter-individual variation. Our results also indicated that all three species have greater variation in foraging habitat use during the post-breeding season compared to the breeding season. Finally, we observed differences in the degree of seasonal shifts in population level diet and consistency in foraging strategies at the individual level across the three gentoo penguin populations examined. This suggests that Pygoscelis penguins can differ in diets and foraging habitat use not only at the population level among species, sites, and seasons, but also in the level of variation within populations, and in the degree of seasonal consistency among individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ainley D (2002) The Adélie penguin: Bellwether of climate change. Columbia University Press, New York

    Book  Google Scholar 

  • Atkinson A, Siegel V, Pakhomov E, Rothery P (2004) Long-term decline in krill stock and increase in salps within the Southern Ocean. Nature 432:100–103. doi:10.1038/nature02996

    Article  CAS  Google Scholar 

  • Barquete V, Strauss V, Ryan PG (2013) Stable isotope turnover in blood and claws: a case study in captive African penguins. J Exp Mar Biol Ecol 448:121–127. doi:10.1016/j.jembe.2013.06.021

    Article  CAS  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. doi:10.1111/j.0021-8790.2004.00861.x

    Article  Google Scholar 

  • Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164. doi:10.3354/meps311157

    Article  Google Scholar 

  • Bolnick DI, Svanback R, Fordyce JA, Yang LH, Davis JM, Hulsey CD, Forister ML (2003) The ecology of individuals: incidence and implications of individual specialization. Am Nat 161:1–28. doi:10.1086/343878

    Article  Google Scholar 

  • Bond AL, Jones IL (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornithol 37:183–188

    Google Scholar 

  • Bugoni L, McGill R, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462. doi:10.1002/rcm.3633

    Article  CAS  Google Scholar 

  • Carleton SA, del Rio CM (2005) The effect of cold-induced increased metabolic rate on the rate of 13C and 15N incorporation in house sparrows (Passer domesticus). Oecologia 144:226–232. doi:10.1007/s00442-005-0066-8

    Article  CAS  Google Scholar 

  • Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bioindicators of mercury contamination in the Southern Ocean: birds from the Kergeulen Islands as a case study. Sci Total Environ 454:141–148. doi:10.1016/j.scitotenv.2013.02.060

    Article  Google Scholar 

  • Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287. doi:10.3354/meps329281

    Article  CAS  Google Scholar 

  • Cherel Y, Hobson KA, Hassani S (2005) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115. doi:10.1086/425202

    Article  Google Scholar 

  • Cherel Y, Jaquemet S, Maglio A, Jaeger A (2014) Differences in δ 13C and δ 15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237. doi:10.1007/s00227-013-2314-5

    Article  Google Scholar 

  • Clarke J, Manly B, Kerry K, Gardner H, Franchi E, Corsolini S, Focardi S (1998) Sex differences in Adélie penguin foraging strategies. Polar Biol 20:248–258. doi:10.1007/s003000050301

    Article  Google Scholar 

  • Clausen AP, Pütz K (2002) Recent trends in diet composition and productivity of gentoo, magellanic and rockhopper penguins in the Falkland Islands. Aquat Conserv 12:51–61. doi:10.1002/aqc.476

    Article  Google Scholar 

  • Clausen A, Pütz K (2003) Winter diet and foraging range of gentoo penguins (Pygoscelis papua) from Kidney Cove, Falkland Islands. Polar Biol 26:32–40. doi:10.1007/s00300-002-0443-2

    Google Scholar 

  • Cruz LL, McGill RA, Goodman SJ, Hamer KC (2012) Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth. Mar Biol 159:873–880. doi:10.1007/s00227-011-1864-7

    Article  CAS  Google Scholar 

  • Dehnhard N, Eens M, Sturaro N, Lepoint G, Demongin L, Quillfeldt P, Poisbleau M (2016) Is individual consistency in body mass and reproductive decisions linked to individual specialization in foraging behavior in a long-lived seabird? Ecol Evol 6:4488–4501. doi:10.1002/ece3.2213

    Article  Google Scholar 

  • Dietrich K, Brooks C, Bystrom I, Driscoll R, Ferm N, Hinke J, Janssen M, Lombard D, Pesce A, Romain S, Thoresen L (2014) Distribution and catch rates of zooplankton around the South Shetland Islands Antarctica. NOAA Techn Memo NMFS SWFSC 524:18–27

    Google Scholar 

  • Dingemanse NJ, Wolf M (2013) Between-individual differences in behavioural plasticity within populations: causes and consequences. Anim Behav 85:1031–1039. doi:10.1016/j.anbehav.2012.12.032

    Article  Google Scholar 

  • Donnelly SM, Kramer A (1999) Testing for multiple species in fossil samples: an evaluation and comparison of tests for equal relative variation. Am J Phys Anthropol 108:507–529. doi:10.1002/(SICI)1096-8644(199904)108:4<507:AID-AJPA8>3.0.CO;2-0

    Article  CAS  Google Scholar 

  • France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312. doi:10.3354/meps124307

    Article  Google Scholar 

  • Gorman KB, Williams TD, Fraser WR (2014) Ecological sexual dimorphism and environmental variability within a community of Antarctic penguins (genus Pygoscelis). PLoS One 9:e90081. doi:10.1371/journal.pone.0090081

    Article  Google Scholar 

  • Handley JM, Connan M, Baylis AMM, Brickle P, Pistorius P (2017) Jack of all prey, master of some: influence of habitat on the feeding ecology of a diving marine predator. Mar Biol 164:82. doi:10.1007/s00227-017-3113-1

    Article  Google Scholar 

  • Hinke JT, Polito MJ, Reiss CS, Trivelpiece SG, Trivelpiece WZ (2012) Flexible reproductive timing can buffer reproductive success of Pygoscelis spp. penguins in the Antarctic Peninsula region. Mar Ecol Prog Ser 454:91–104. doi:10.3354/meps09633

    Article  Google Scholar 

  • Hinke JT, Polito MJ, Goebel ME, Jarvis S, Reiss CS, Thorrold SR, Trivelpiece WZ, Watters GM (2015) Spatial and isotopic niche partitioning during winter in chinstrap and Adélie penguins from the South Shetland Islands. Ecosphere 6:1–32. doi:10.1890/ES14-00287.1

    Article  Google Scholar 

  • Hobson KA, Bond AL (2012) Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses. Mar Ecol Prog Ser 461:233–243. doi:10.3354/meps09835

    Article  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes I: turnover of 13C in tissues. Condor 94:181–188. doi:10.2307/1368807

    Article  Google Scholar 

  • Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798. doi:10.2307/5256

    Article  Google Scholar 

  • Hückstädt LA, Koch PL, McDonald BI, Goebel ME, Crocker DE, Costa DP (2012) Stable isotope analyses reveal individual variability in the trophic ecology of a top marine predator, the southern elephant seal. Oecologia 169:395–406. doi:10.1007/s00442-011-2202-y

    Article  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602. doi:10.1111/j.1365-2656.2011.01806.x

    Article  Google Scholar 

  • Jarman SN, McInnes JC, Faux C, Polanowski AM, Marthick J, Deagle BE, Southwell C, Emmerson L (2013) Adélie penguin population diet monitoring by analysis of food DNA in scats. PLoS One 8:e82227. doi:10.1371/journal.pone.0082227

    Article  Google Scholar 

  • Juáres MA, Santos M, Mennucci JA, Coria NR, Mariano-Jelicich R (2016) Diet composition and foraging habitats of Adélie and gentoo penguins in three different stages of their annual cycle. Mar Biol 163:105. doi:10.1007/s00227-016-2886-y

    Article  Google Scholar 

  • Karnovsky NJ (1997) The fish component of Pygoscelis penguin diets. Dissertation, Montana State University-Bozeman, College of Letters and Science

  • Kernaléguen L, Dorville N, Ierodiaconou D, Hoskins AJ, Baylis AMM, Hindell MA, Semmens J, Abernathy K, Marshall GJ, Cherel Y, Arnould JPY (2016) From video recordings to whisker stable isotopes: a critical evaluation of timescale in assessing individual foraging specialization in Australian fur seals. Oecologia 180:657–670. doi:10.1007/s00442-015-3407-2

    Article  Google Scholar 

  • Kohler SA, Connan M, Hill JM, Mablouke C, Bonnevie B, Ludynia K, Kemper J, Huisamen J, Underhill LG, Cherel Y, McQuaid Jaquemet S (2011) Geographic variation in the trophic ecology of an avian rocky shore predator, the African black oystercatcher, along the southern African coastline. Mar Ecol Prog Ser 435:235–249. doi:10.3354/meps09215

    Article  Google Scholar 

  • Lascara CM, Hofmann EE, Ross RM, Quetin LB (1999) Seasonal variability in the distribution of Antarctic krill, Euphausia superba, west of the Antarctic Peninsula. Deep Sea Res Part 1(46):951–984. doi:10.1016/S0967-0637(98)00099-5

    Article  Google Scholar 

  • Lescroël A, Bost CA (2005) Foraging under contrasting oceanographic conditions: the gentoo penguin at Kerguelen Archipelago. Mar Ecol Progr Ser 302:245–261. doi:10.3354/meps302245

    Article  Google Scholar 

  • Lescroël A, Ridoux V, Bost CA (2004) Spatial and temporal variation in the diet of the gentoo penguin (Pygoscelis papua) at Kerguelen Islands. Polar Biol 27:206–216. doi:10.1007/s00300-003-0571-3

    Article  Google Scholar 

  • Lishman GS (1985) The food and feeding ecology of Adélie penguins (Pygoscelis adeliae) and chinstrap penguins (Pygoscelis antarctica) at Signy Island, South Orkney Islands. J Zool 205:245–263. doi:10.1016/S0967-0637(98)00099-5

    Article  Google Scholar 

  • Lynch HJ, Naveen R, Casanovas P (2013) Antarctic site inventory breeding bird survey data, 1994-1013. Ecology 94:2653. doi:10.1890/13-1108.1

    Article  Google Scholar 

  • Miller AK, Trivelpiece WZ (2008) Chinstrap penguins alter foraging and diving behavior in response to the size of their principal prey, Antarctic krill. Mar Biol 154:201–208. doi:10.1007/s00227-008-0909-z

    Article  Google Scholar 

  • Miller AK, Karnovsky NJ, Trivelpiece WZ (2009) Flexible foraging strategies of gentoo penguins Pygoscelis papua over 5 years in the South Shetland Islands, Antarctica. Mar Biol 156:2527–2537. doi:10.1007/s00227-009-1277-z

    Article  Google Scholar 

  • Miller AK, Kappes MA, Trivelpiece SG, Trivelpiece WZ (2010) Foraging-niche separation of breeding gentoo and chinstrap penguins, South Shetland Islands, Antarctica. Condor 112:683–695. doi:10.1525/cond.2010.090221

    Article  Google Scholar 

  • Minagawa M, Wada E (1984) Stepwise enrichment of 15 N along food chains: further evidence and the relation between δ15 N and animal age. Geochim Cosmochim Acta 48:1135–1140. doi:10.1016/0016-7037(84)90204-7

    Article  CAS  Google Scholar 

  • Negrete P, Sallaberry M, Barceló G, Maldonado K, Perona F, McGill RA, Quillfeldt P, Sabat P (2016) Temporal variation in isotopic composition of Pygoscelis penguins at Ardley Island, Antarctic: are foraging habits impacted by environmental change? Polar Biol 3:1–4. doi:10.1007/s00300-016-2017-8

    Google Scholar 

  • Newsome SD, Martínez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436. doi:10.1890/060150.1

    Article  Google Scholar 

  • Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974. doi:10.1890/07-1812.1

    Article  Google Scholar 

  • Orsi AH, Harris U (2015) Locations of the various fronts in the Southern Ocean Australian Antarctic Data Centre—CAASM Metadata. https://data.aad.gov.au/metadata/records/southern_ocean_fronts. Accessed 20 May 2016

  • Polito MJ, Trivelpiece WZ (2008) Transition to independence and evidence of extended parental care in the gentoo penguin (Pygoscelis papua). Mar Biol 154:231. doi:10.1007/s00227-008-0919-x

    Article  Google Scholar 

  • Polito MJ, Fisher S, Tobias CR, Emslie SD (2009) Tissue-specific isotopic discrimination factors in gentoo penguin (Pygoscelis papua) egg components: implications for dietary reconstruction using stable isotopes. J Exp Mar Biol Ecol 372:106–112. doi:10.1016/j.jembe.2009.02.014

    Article  CAS  Google Scholar 

  • Polito MJ, Abel S, Tobias CR, Emslie SD (2011a) Dietary isotopic discrimination in gentoo penguin (Pygoscelis papua) feathers. Polar Biol 34:1057–1063. doi:10.1007/s00300-011-0966-5

    Article  Google Scholar 

  • Polito MJ, Abel S, Lynch HJ, Naveen R, Emslie SD (2011b) Stable isotopes reveal regional heterogeneity in the pre-breeding distribution and diets of sympatrically breeding Pygoscelis spp. penguins. Mar Ecol Prog Ser 421:265–277. doi:10.3354/meps08863

    Article  Google Scholar 

  • Polito MJ, Trivelpiece WZ, Karnovsky NJ, Ng E, Patterson WP, Emslie SD (2011c) Integrating stomach content and stable isotope analyses to quantify the diets of Pygoscelid penguins. PLoS One 6:e26642. doi:10.1371/journal.pone.0026642

    Article  CAS  Google Scholar 

  • Polito MJ, Clucas GV, Hart T, Trivelpiece WZ (2012) A simplified method of determining the sex of Pygoscelis penguins using bill measurements. Mar Ornithol 40:89–94

    Google Scholar 

  • Polito MJ, Reiss CS, Trivelpiece WZ, Patterson WP, Emslie SD (2013) Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica. Mar Biol 160:1311–1323. doi:10.1007/s00227-013-2182-z

    Article  Google Scholar 

  • Polito MJ, Trivelpiece WZ, Patterson WP, Karnovsky NJ, Reiss CS, Emslie SD (2015) Contrasting specialist and generalist patterns facilitate foraging niche partitioning in sympatric populations of Pygoscelis penguins. Mar Ecol Prog Ser 519:221–237. doi:10.3354/meps11095

    Article  CAS  Google Scholar 

  • Pütz K, Ingham RJ, Smith JG, Croxall JP (2001) Population trends, breeding success and diet composition of gentoo Pygoscelis papua, magellanic Spheniscus magellanicus and rockhopper Eudyptes chrysocome penguins in the Falkland Islands. A review. Polar Biol 24:793–807. doi:10.1007/s003000100293

    Article  Google Scholar 

  • Quillfeldt P, Bugoni L, McGill RA, Masello JF, Furness RW (2008) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598. doi:10.1007/s00227-008-1048-2

    Article  CAS  Google Scholar 

  • R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.r-project.org

  • Sanpera C, Ruizi X, Moreno R, Jover L, Waldron S (2007) Mercury and stable isotopes in feathers of Audouin’s gulls as indicators of feeding habits and migratory connectivity. Condor 109:268–275. doi:10.1650/0010-5422(2007)109[268:MASIIF]2.0.CO;2

    Article  Google Scholar 

  • Sargeant BL (2007) Individual foraging specialization: niche width versus niche overlap. Oikos 116:1431–1437. doi:10.1111/j.0030-1299.2007.15833.x

    Article  Google Scholar 

  • Trivelpiece WZ, Trivelpiece SG, Volkman NJ (1987) Ecological segregation of Adélie, gentoo, and chinstrap penguins at King George Island, Antarctica. Ecology 68:351–361. doi:10.2307/1939266

    Article  Google Scholar 

  • Trivelpiece WZ, Hinke JT, Miller AK, Reiss CS, Trivelpiece SG, Watters GM (2011) Variability in krill biomass links harvesting and climate warming to penguin population changes in Antarctica. Proc Natl Acad Sci USA 108:7625–7628. doi:10.1073/pnas.1016560108

    Article  CAS  Google Scholar 

  • Volkman NJ, Presler P, Trivelpiece WZ (1980) Diets of Pygoscelid penguins at King George Island, Antarctica. Condor 82:373–378

    Article  Google Scholar 

  • Wilson RP (2010) Resource partitioning and niche hyper-volume overlap in free-living Pygoscelid penguins. Funct Ecol 24:646–657. doi:10.1111/j.1365-2435.2009.01654.x

    Article  Google Scholar 

  • Wilson RP, Alvarrez B, Latorre L, Adelung D, Culik B, Bannasch R (1998) The movements of gentoo penguins Pygoscelis papua from Ardley Island, Antarctica. Polar Biol 19:407–413. doi:10.1007/s003000050266

    Article  Google Scholar 

  • Woo KJ, Elliott KH, Davidson M, Gaston AJ, Davoren GK (2008) Individual specialization in diet by a generalist marine predator reflects specialization in foraging behaviour. J Anim Ecol 77:1082–1091. doi:10.3354/meps0722

    Article  Google Scholar 

Download references

Acknowledgements

Many thanks to K. Boysen, P. Chilton, G. Clucas, S. Trivelpiece, A. Will and all field workers who helped to collect the samples used in this study. Funding was provided in part by a NSF Office of Polar Programs grant to S. Emslie and M. Polito (ANT-0739575). We would like to acknowledge support from the Department of Oceanography and Coastal Sciences at Louisiana State University, the CAPES foundation (PDSE scholarship No 6406/2015-07) the Darwin Initiative and public donations during this fieldwork. We also thank the US-AMLR and PROANTAR program, Brazilian Institute INCT-APA, Raytheon Polar Services, Quark Expeditions, the Laurence M. Gould, the M/V Ushuaia, M/V Ocean Diamond for transportation and logistical support. We thank Steve Emslie for assistance with permitting and sample shipping and T. Mauney who provided assistance with sample preparation and stable isotope analysis. We thank Y. Cherel, N. Dehnhard, A. Satake, M. Harvey, and an anonymous reviewer for helpful comments on earlier versions of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Rachael W. Herman.

Ethics declarations

Conflict of interest

The authors declare that they have no conflicts of interest.

Human and animal ethics

Animal use in this study was conducted under approved animal use protocols from the University of North Carolina Wilmington (A0910-20) and Louisiana State University (14-083), the Universidade do Vale do Rio dos Sinos (CNPq: No 574018/2008-5 and FAPERJ: No E-16/170.023/2008), Technology and Innovation (MCTI), of Environment (MMA) and Inter-Ministry Commission for Sea Resources (CIRM) and in accordance to Antarctic Conservation Act permits provided by the U.S. National Science Foundation (NSF) to G. Watters (2011–005) and M. Polito (2015–008).

Additional information

Responsible Editor: Y. Cherel.

Reviewed by N. Dehnhard and an undisclosed expert.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Herman, R.W., Valls, F.C.L., Hart, T. et al. Seasonal consistency and individual variation in foraging strategies differ among and within Pygoscelis penguin species in the Antarctic Peninsula region. Mar Biol 164, 115 (2017). https://doi.org/10.1007/s00227-017-3142-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3142-9

Keywords

Navigation