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Physiological constraints and the influence of diet on fatty acids in the yolk of gentoo penguins, Pygoscelis papua

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Abstract

Avian yolk fatty acids (FA) composition is influenced by two main factors: maternal diet and genetic factors that regulate FA metabolism. However, due to embryonic developmental requirements, yolk FA are thought to be physiologically constrained and less useful for dietary and trophic studies. We assessed the relative contributions of diet and physiological constraints in determining the yolk FA composition of a marine bird, the gentoo penguin (Pygoscelis papua) by comparing FA signatures of yolks and prey between a captive, controlled- feeding experiment and a wild population. Captive and wild yolk FA signatures differed even though both groups’ yolk lipids were composed primarily of three FA (16:0, 18:0 and 18:1n-9). Differences were due to FA occurring in relatively low abundance, but which mirrored differences in the FA composition of diets. However, yolk FA signatures were correlated across three penguin species suggesting that common developmental constraints can be relatively more important than species-specific differences in diet or egg-laying physiology. While yolk FA are constrained, several minor components of yolk FA are reflective of diets and the calibration coefficients resulting from this study have the potential to be incorporated into predictive models and allow for quantitative dietary and trophic studies using FA analysis of penguin egg yolks.

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References

  • Anderson GJ, Connor WE, Corliss JD, Lin DS (1989) Rapid modulation of the n-3 docosahexaenoic acid levels in the brain and retina of the newly hatched chick. J Lipid Res 30:433–441

    PubMed  CAS  Google Scholar 

  • Astheimer LB, Grau CR (1990) A comparison of yolk growth-rates in seabird eggs. Ibis 132:380–394

    Article  Google Scholar 

  • Barrett RT, Camphuysen K, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Huppop O, Leopold MF, Montevecchi WA, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691

    Article  Google Scholar 

  • Barton NWH, Fox NC, Surai PF, Speake BK (2002) Vitamins E and A, carotenoids, and fatty acids of the raptor egg yolk. J Raptor Res 36:33–38

    Google Scholar 

  • Boyd I, Wanless S, Camphuysen CJ (eds) (2006) Top predators in marine ecosystems: their role in monitoring and management. Cambridge University Press, Cambridge

    Google Scholar 

  • Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349

    Article  Google Scholar 

  • Bremer J, Norum KR (1982) Metabolism of very long-chain monounsaturated fatty-acids (22:1) and the adaptation to their presence in the diet. J Lipid Res 23:243–256

    PubMed  CAS  Google Scholar 

  • Brown DJ, Boyd IL, Cripps GC, Butler PJ (1999) Fatty acid signature analysis from the milk of Antarctic fur seals and Southern elephant seals from South Georgia: implications for diet determination. Mar Ecol Prog Ser 187:251–263

    Article  CAS  Google Scholar 

  • Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Mar Mammal Sci 22:759–801

    Article  Google Scholar 

  • Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER, vers. 6: user manual/tutorial, PRIMER-E, Plymouth, UK

  • Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation. PRIMER-E, Plymouth

    Google Scholar 

  • Connan M, Mayzaud P, Duhamel G, Bonnevie BT, Cherel Y (2010) Fatty acid signature analysis documents the diet of five myctophid fish from the Southern Ocean. Mar Biol 157:2303–2316

    Article  CAS  Google Scholar 

  • Cooper MH, Iverson SJ, Rouvinen-Watt K (2006) Metabolism of dietary cetoleic acid (22: 1n–11) in mink (Mustela vison) and gray seals (Halichoerus grypus) studied using radiolabeled fatty acids. Physiol Biochem Zool 79:820–829

    Article  PubMed  CAS  Google Scholar 

  • Decrock F, Groscolas R, McCartney RJ, Speake BK (2001) Transfer of n-3 and n-6 polyunsaturated fatty acids from yolk to embryo during development of the king penguin. Am J Physiol-Reg I 280:R843–R853

    CAS  Google Scholar 

  • Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  • Groscolas R (1990) Metabolic adaptations to fasting in emperor and king penguins. In: Davis LS, Darby JT (eds) Penguin Biology. Academic Press, London, pp 269–296

    Google Scholar 

  • Groscolas R, Frechard F, Decrock F, Speake BK (2003) Metabolic fate of yolk fatty acids in the developing king penguin embryo. Am J Physiol-Reg I 285:R850–R861

    CAS  Google Scholar 

  • Hilditch TP, Williams PN (1964) The chemical constitution of natural fats. Chapman & Hall, London

    Google Scholar 

  • Hintze J (2004) NCSS and PASS. Number Cruncher Statistical System, Kaysville, Utah

  • Iverson SJ (1993) Milk secretion in marine mammals in relation to foraging: can milk fatty acids predict diet? Sym Zool Soc Lond 66:263–291

    Google Scholar 

  • Iverson SJ (2009) Tracing aquatic food webs using fatty acids: from qualitative indicators to quantitative determination. In: Kainz M, Brett MT, Arts MT (eds) Lipids in Aquatic Ecosystems. Springer, New York, pp 281–308

    Chapter  Google Scholar 

  • Iverson SJ, Lang SLC, Cooper MH (2001) Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283–1287

    Article  PubMed  CAS  Google Scholar 

  • Iverson SJ, Frost KJ, Lang SLC (2002) Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: factors contributing to among and within species variability. Mar Ecol Prog Ser 241:161–181

    Article  CAS  Google Scholar 

  • Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol Monogr 74:211–235

    Article  Google Scholar 

  • Iverson SJ, Springer AM, Kitaysky AS (2007) Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Mar Ecol Prog Ser 352:235–244

    Article  CAS  Google Scholar 

  • Käkelä R, Furness RW, Kahle S, Becker PH, Käkelä A (2009) Fatty acid signatures in seabird plasma are a complex function of diet composition: a captive feeding trial with herring gulls. Funct Ecol 23:141–149

    Article  Google Scholar 

  • Käkelä R, Käkelä A, Martinez-Abrain A, Sarzo B, Louzao M, Gerique C, Villuendas E, Strandberg U, Furness RW, Oro D (2010) Fatty acid signature analysis confirms foraging resources of a globally endangered Mediterranean seabird species: calibration test and application to the wild. Mar Ecol Prog Ser 398:245–258

    Article  Google Scholar 

  • Koopman HN (2007) Phylogenetic, ecological, and ontogenetic factors influencing the biochemical structure of the blubber of odontocetes. Mar Biol 151:277–291

    Article  Google Scholar 

  • Lane HA, Westgate AJ, Koopman HK (2010) Ontogenetic and temporal variability in the fat content and fatty acid composition of Atlantic herring (Clupea harengus) from the Bay of Fundy, Canada. Fish Bull 109(1):113–122

    Google Scholar 

  • Lipar JL, Ketterson ED, Nolan V (1999) Intraclutch variation in testosterone content of red-winged blackbird eggs. Auk 116:231–235

    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

    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

    Article  Google Scholar 

  • Miyazaki M, Ntambi JM (2008) Fatty acid desaturation and chain elongation in mammals. In: Vance D, Vance J (eds) Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam, pp 191–211

    Chapter  Google Scholar 

  • Offredo C, Ridoux V (1986) The diet of emperor penguins Aptenodytes forsteri in Adélie Land, Antarctica. Ibis 128:409–413

    Article  Google Scholar 

  • Oppel S, Powell AN, O’Brien DM (2010) King eiders use an income strategy for egg production: a case study for incorporating individual dietary variation into nutrient allocation research. Oecologia 164:1–12

    Article  PubMed  Google Scholar 

  • Raclot T (2003) Selective mobilization of fatty acids from adipose tissue triacylglycerols. Prog Lipid Res 42:257–288

    Article  PubMed  CAS  Google Scholar 

  • Raclot T, Groscolas R, Cherel Y (1998) Fatty acid evidence for the importance of myctophid fishes in the diet of king penguins, Aptenodytes patagonicus. Mar Biol 132:523–533

    Article  Google Scholar 

  • Ronconi RA, Koopman HN, McKinstry CAE, Wong SNP, Westgate AJ (2010) Inter-annual variability in diet of non-breeding pelagic seabirds Puffinus spp. at migratory staging areas: evidence from stable isotopes and fatty acids. Mar Ecol Prog Series 419:267–282

    Article  Google Scholar 

  • Speake BK, Murray AMB, Noble RC (1998) Transport and transformations of yolk lipids during development of the avian embryo. Prog Lipid Res 37:1–32

    Article  PubMed  CAS  Google Scholar 

  • Speake BK, Decrock F, Surai PF, Groscolas R (1999a) Fatty acid composition of the adipose tissue and yolk lipids of a bird with a marine-based diet, the emperor penguin (Aptenodytes forsteri). Lipids 34:283–290

    Article  PubMed  CAS  Google Scholar 

  • Speake BK, Surai PF, Noble RC, Beer JV, Wood NAR (1999b) Differences in egg lipid and antioxidant composition between wild and captive pheasants and geese. Comp Biochem Physiol B 124:101–107

    Article  Google Scholar 

  • Speake BK, Surai PF, Bortolotti GR (2002) Fatty acid profiles of yolk lipids of five species of wild ducks (Anatidae) differing in dietary preference. J Zool 257:533–538

    Article  Google Scholar 

  • Sprecher H, Luthria DL, Mohammed BS, Baykousheva SP (1995) Reevaluation of the pathways for the biosynthesis of polyunsaturated fatty acids. J Lipid Res 36:2471–2477

    PubMed  CAS  Google Scholar 

  • Surai PF, Speake BK (2008) The natural fatty acid compositions of eggs of wild birds and the consequences of domestication. In: Meester F, Watson RR (eds) Wild-Type food in health promotion and disease prevention: the columbus concept. Humana Press, Totowa, pp 121–137

    Chapter  Google Scholar 

  • Surai PF, Bortolotti GR, Fidgett AL, Blount JD, Speake BK (2001) Effects of piscivory on the fatty acid profiles and antioxidants of avian yolk: studies on eggs of the gannet, skua, pelican and cormorant. J Zool 255:305–312

    Article  Google Scholar 

  • Tierney M, Nichols PD, Wheatley KE, Hindell MA (2008) Blood fatty acids indicate inter- and intra-annual variation in the diet of Adelie penguins: comparison with stomach content and stable isotope analysis. J Exp Mar Biol Ecol 367:65–74

    Article  CAS  Google Scholar 

  • Trivelpiece WZ, Trivelpiece SG (1990) Courtship period of Adélie, gentoo and chinstrap penguins. In: Davis LS, Darby JT (eds) Penguin biology. Academic Press, London, pp 113–130

    Google Scholar 

  • Ulberth F, Gabernig RG, Schrammel F (1999) Flame-ionization detector response to methyl, ethyl, propyl, and butyl esters of fatty acids. J Am Oil Chem Soc 76:263–266

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Wang SW, Hollmen TE, Iverson SJ (2010) Validating quantitative fatty acid signature analysis to estimate diets of spectacled and Steller’s eiders (Somateria fischeri and Polysticta stelleri). J Comp Physiol B 180:125–139

    Article  PubMed  CAS  Google Scholar 

  • Williams CT, Buck CL (2010) Using fatty acids as dietary tracers in seabird trophic ecology: theory, application and limitations. J Ornithol 151:531–543

    Article  Google Scholar 

  • Williams CT, Iverson SJ, Buck CL (2009) The effects of diet and caloric restriction on adipose tissue fatty acid signatures of tufted puffin (Fratercula cirrhata) nestlings. J Comp Physiol B 179:711–720

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank K. Vires, J. Beck, K. McGrath, T. Solberg and D. Rivard and the staff of the Scott Kingdoms of the Seas Aquarium for their helpful assistance with this study. Thank you to H. Lynch, R. Naveen, M. Rider, Oceanites Inc., Raytheon Polar Services and Linblad Expeditions for invaluable logistical support in Antarctica. We thank the US AMLR program and A. VanCise for access to krill samples and S. Wang for insights on sea-duck yolk FA. H. Lane and C. McKinstry provided for assistance with lipid extractions and statistical analyses. Thank you to A. Satake and two anonymous reviewers for helpful comments during the preparation of this manuscript. This research was funded by U.S. National Science Foundation (NSF) Office of Polar Programs (OPP) grants ANT-0125098 and ANT-0739575 to S. Emslie, and completed in accordance to animal use permits provided by Omaha’s Henry Doorly Zoo (HDZ#07-800) and NSF OPP (ACA 2006-001).

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Authors and Affiliations

  1. Department of Biology and Marine Biology, University of North Carolina Wilmington, 601 South College Road, Wilmington, NC, 28403, USA

    Michael J. Polito & Heather N. Koopman

  2. Omaha’s Henry Doorly Zoo, 3701 South 10th Street, Omaha, NE, 68107, USA

    Stephanie Able

  3. Antarctic Ecosystem Research Division, NOAA-NMFS, Southwest Fisheries Science Center, 8604 La Jolla Shores Drive, La Jolla, CA, 92037-1508, USA

    Jennifer Walsh & Michael E. Goebel

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  1. Michael J. Polito
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  2. Heather N. Koopman
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Correspondence to Michael J. Polito.

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Communicated by I. D. Hume.

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Polito, M.J., Koopman, H.N., Able, S. et al. Physiological constraints and the influence of diet on fatty acids in the yolk of gentoo penguins, Pygoscelis papua . J Comp Physiol B 182, 703–713 (2012). https://doi.org/10.1007/s00360-012-0649-8

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