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Marine Biology

, Volume 162, Issue 3, pp 501–514 | Cite as

Foraging effort in Magellanic penguins: balancing the energy books for survival?

  • J. E. SalaEmail author
  • R. P. Wilson
  • F. Quintana
Original Paper

Abstract

The determination of activity-specific energy expenditure of wild animals is key in ecology and conservation sciences. Energy management is crucial for seabirds during the breeding season when they need to maintain a positive balance between energy intake and the metabolic costs for them and their young. We analysed information from accelerometers to estimate the energy expenditure of Magellanic penguins (Spheniscus magellanicus) foraging at sea during the early chick-rearing period from four Patagonian colonies (i.e. Punta Norte, Bahía Bustamante, Puerto Deseado and Puerto San Julián). We studied how activity-specific energy consumption affected total energy expenditure during foraging and considered how this related to the current status and trends of breeding populations. The derived diving energy expenditure of penguins differed between sites, with inter-colony differences being primarily due to variability during the bottom and ascent phases of the dives: bottom phase energy expenditure was largely determined by the total distances travelled during the search, pursuit, and capture of prey, rather than the time per se allocated to this phase. Those colonies where the rate of population change was lowest also expended the most energy per trip due to greater times spent underwater and/or undertaking a higher number of dives per trip. Finally, the total energy consumption as well as the rate of energy expenditure per trip was good indicators of trends in breeding populations.

Keywords

Total Energy Expenditure Daily Diary Bottom Phase Metabolic Power Estimate Energy Expenditure 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

Research was funded by grants from the Wildlife Conservation Society (WCS), Consejo Nacional de Investigaciones Científicas y Técnicas de la República Argentina (CONICET), and Agencia Nacional de Promoción Científica y Tecnológica to FQ and by a Rolex Award for Enterprise awarded to RPW. We want to thank the POGO (Partnership for Observation of the Global Oceans, http://www.ocean-partners.org/) for the award to Juan Emilio Sala to enable him to conduct a training period at Swansea University (2010). We want to especially thank A. Gómez-Laich for her invaluable assistance in statistical analysis using R. We also thank the respective Conservation Agencies from the provinces of Chubut and Santa Cruz for the permits to work in the different protected areas, and the Centro Nacional Patagónico (CENPAT-CONICET) for institutional and logistical support. J. E. Sala is supported by a postdoctoral fellowship from CONICET. Finally, we particularly thank those anonymous reviewers who provided valuable comments and contributed to a significant improvement of this paper and to Dr. Lorien Pichegru for her positive approach to refereeing and the abtterment of science.

References

  1. Acha EM, Mianzan HW, Guerrero RA et al (2004) Marine fronts at the continental shelves of austral South America: physical and ecological processes. J Mar Syst 44:83–105CrossRefGoogle Scholar
  2. Ballance LT, Ainley DG, Ballard G, Barton K (2009) An energetic correlate between colony size and foraging effort in seabirds, an example of the Adélie penguin Pygoscelis adeliae. J Avian Biol 40:279–288CrossRefGoogle Scholar
  3. Bannasch R, Wilson RP, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J Exp Biol 194:83–96Google Scholar
  4. BirdLife International (2013) Species factsheet: Spheniscus magellanicus. http://www.birdlife.org
  5. Boersma PD, Rebstock GA (2009) Foraging distance affects reproductive success in Magellanic penguins. Mar Ecol Prog Ser 375:263–275CrossRefGoogle Scholar
  6. Boersma PD, Rebstock GA, Frere E, Moore SE (2009) Following the fish: penguins and productivity in the South Atlantic. Ecol Monogr 79:59–76CrossRefGoogle Scholar
  7. Bost CA, Handrich Y, Butler PJ et al (2007) Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep-Sea Res II 54:248–255CrossRefGoogle Scholar
  8. Boswall J, MacIver D (1975) The Magellanic penguin Spheniscus magellanicus. In: Stonehouse B (ed) The biology of penguins. Macmillan, London, pp 271–305Google Scholar
  9. Brown JH, Gilloly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  11. Crawley MJ (2007) The R Book. Wiley, West SussexCrossRefGoogle Scholar
  12. Forero MG, Tella JL, Hobson KA et al (2002) Conspecific food competition explains variability in colony size: a test using stable isotopes in Magellanic penguins. Ecology 83:3466–3475CrossRefGoogle Scholar
  13. Gandini PA, Frere E, Pettovello AD, Cedrola PV (1999) Interaction between Magellanic penguins and shrimp fisheries in Patagonia, Argentina. Condor 101:783–789CrossRefGoogle Scholar
  14. Gleiss AC, Wilson RP, Shepard ELC (2011) Making overall dynamic body acceleration work: on the theory of acceleration as a proxy for energy expenditure. Methods Ecol Evol 2:23–33CrossRefGoogle Scholar
  15. Gómez-Laich A, Wilson RP, Quintana F, Shepard ELC (2008) Identification of imperial cormorant Phalacrocorax atriceps behaviour using accelerometers. Endanger Species Res 10:29–37CrossRefGoogle Scholar
  16. Gómez-Laich A, Wilson RP, Gleiss AC et al (2011) Use of overall dynamic body acceleration for estimating energy expenditure in cormorants; does locomotion in different media affect relationships? J Exp Mar Biol Ecol 399:151–155CrossRefGoogle Scholar
  17. Gómez-Laich A, Wilson RP, Shepard ELC, Quintana F (2013) Energy expenditure and food consumption of foraging Imperial cormorants in Patagonia, Argentina. Mar Biol 160:1697–1707CrossRefGoogle Scholar
  18. Green JA, Halsey LG, Wilson RP, Frappell PB (2009) Estimating energy expenditure of animals using the accelerometry technique: activity, inactivity and comparison with the heart-rate technique. J Exp Biol 212:471–482CrossRefGoogle Scholar
  19. Grémillet D, Charmantier A (2010) Shifts in phenotypic plasticity constrain the value of seabirds as ecological indicators of marine ecosystems. Ecol Appl 20:1498–1503. doi: 10.1890/09-1586.1 CrossRefGoogle Scholar
  20. Grémillet D, Pichegru L, Siorat F, Georges JY (2006) Conservation implications of the apparent mismatch between population dynamics and foraging effort in French northern gannets from the English Channel. Mar Ecol Prog Ser 319:15–25CrossRefGoogle Scholar
  21. Halsey L (2011) The challenge of measuring energy expenditure: current field and laboratory methods. Comp Biochem Physiol Part A 158:247–251CrossRefGoogle Scholar
  22. Halsey L, Woakes A, Butler P (2003) Testing optimal foraging models for air-breathing divers. Anim Behav 65:641–653CrossRefGoogle Scholar
  23. Halsey LG, Shepard ELC, Gómez-Laich A et al (2009a) The relationship between oxygen consumption and body acceleration in a range of species. Comp Biochem Physiol A 152:197–202CrossRefGoogle Scholar
  24. Halsey LG, Green AJ, Wilson RP, Frappell PB (2009b) Accelerometry to estimate energy expenditure during activity: best practice with data loggers. Physiol Biochem Zool 82:396–404CrossRefGoogle Scholar
  25. Hanuise N, Bost CA, Huin W et al (2010) Measuring foraging activity in a deep-diving bird: comparing wiggles, oesophageal temperatures and beak-opening angles as proxies of feeding. J Exp Biol 213:3874–3880CrossRefGoogle Scholar
  26. Harris S, Quintana F, Rey AR (2012) Prey search behavior of the Imperial Cormorant (Phalacrocorax atriceps) during the breeding season at Punta León, Argentina. Waterbirds 35:312–323CrossRefGoogle Scholar
  27. Hennicke JC, Culik BM (2005) Foraging performance and reproductive success of Humboldt penguins in relation to prey availability. Mar Ecol Prog Ser 296:173–181CrossRefGoogle Scholar
  28. Langton R, Davies IM, Scott BE (2011) Seabird conservation and tidal stream and wave power generation: information needs for predicting and managing potential impacts. Mar Policy 35:623–630CrossRefGoogle Scholar
  29. Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819CrossRefGoogle Scholar
  30. Lewis S, Grémillet D, Daunt F et al (2006) Using behavioural and state variables to identify proximate causes of population change in a seabird. Oecologia 147:606–614CrossRefGoogle Scholar
  31. Lewison R, Oro D, Godley BJ et al (2012) Research priorities for seabirds: improving conservation and management in the 21st century. Endanger Species Res 17:93–121CrossRefGoogle Scholar
  32. Luna-Jorquera G, Culik BM (1999) Diving behaviour of Humboldt Penguins Spheniscus humboldti in northern Chile. Mar Ornithol 27:67–76Google Scholar
  33. Luna-Jorquera G, Culik BM (2000) Metabolic rates of swimming Humboldt penguins. Mar Ecol Prog Ser 203:301–309CrossRefGoogle Scholar
  34. Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. Ohio State University Press, Columbus, pp 154–177Google Scholar
  35. Pastous Madureira PLS, Castello JP, Prentice-Hernández C, et al. (2009) Current and potential alternative food uses of the Argentine anchoita (Engraulis anchoita) in Argentina, Uruguay and Brazil. In: Hasan MR, Halwart M (eds) Fish as feed inputs for aquaculture: practices, sustainability and implications. FAO Fisheries and Aquaculture Technical Paper. No. 518. Rome, pp 269-287Google Scholar
  36. Peters G, Wilson RP, Scolaro JA et al (1998) The diving behavior of Magellanic Penguins at Punta Norte, Península Valdés, Argentina. Waterbirds 21:1–10CrossRefGoogle Scholar
  37. Petersen SL, Ryan PG, Gremillet D (2006) Is food availability limiting African penguins Spheniscus demersus at Boulders? A comparison of foraging effort at mainland and island colonies. Ibis 148:14–26CrossRefGoogle Scholar
  38. Pimm SL, Jenkins CN, Abell R et al (2014) The biodiversity of species and their rates of extinction, distribution, and protection. Science 344(6187):1246752. doi: 10.1126/science.1246752 CrossRefGoogle Scholar
  39. Pyke GH (1984) Optimal foraging theory: a critical review. A Rev Ecol Syst 15:523–575CrossRefGoogle Scholar
  40. Qasem L, Cardew A, Wilson A et al (2012) Tri-axial dynamic acceleration as a proxy for animal energy expenditure; should we be summing values or calculating the vector? PLoS ONE 7(2):e31187. doi: 10.1371/journal.pone.0031187 CrossRefGoogle Scholar
  41. Quintana F, Dell´Arciprete P, Copello S (2010) Foraging behaviour and habitat use by the Southern Giant Petrel on the Patagonian Shelf. Mar Biol 157:515–525CrossRefGoogle Scholar
  42. Quintana F, Wilson R, Dell´Arciprete P et al (2011) Women are from Venus, men from Mars: how may intersex foraging difference be expressed in colonial cormorants? Oikos 120:350–358CrossRefGoogle Scholar
  43. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  44. Rey AR, Bost CA, Schiavini A, Pütz K (2010) Foraging movements of Magellanic penguins Spheniscus magellanicus in the Beagle Channel, Argentina, related to tide and tidal currents. J Ornithol 151:933–943CrossRefGoogle Scholar
  45. Rey AR, Pütz K, Scioscia G et al (2012) Sexual differences in the foraging behaviour of Magellanic Penguins related to stage of breeding. Emu 112:90–96CrossRefGoogle Scholar
  46. Rivas AL, Dogliotti AI, Gagliardini DA (2006) Seasonal variability in satellite-measured surface chlorophyll in the Patagonian Shelf. Cont Shelf Res 26:703–720CrossRefGoogle Scholar
  47. Ropert-Coudert Y, Wilson RP, Daunt F, Kato A (2004) Patterns of energy acquisition by a central place forager: benefits of alternating short and long foraging trips. Behav Ecol 15:824–830CrossRefGoogle Scholar
  48. Sala JE, Wilson RP, Quintana F (2012a) How much is too much? Assessment of prey consumption by Magellanic penguins in Patagonian colonies. PLoS ONE 7(12):e51487. doi: 10.1371/journal.pone.0051487 CrossRefGoogle Scholar
  49. Sala JE, Wilson RP, Frere E, Quintana F (2012b) Foraging effort in Magellanic penguins in Coastal Patagonia, Argentina. Mar Ecol Prog Ser 464:273–287. doi: 10.3354/meps09887 CrossRefGoogle Scholar
  50. Sala JE, Quintana F, Frere E, Wilson RP (2014) Flexible foraging for finding fish: variable diving patterns in Magellanic penguins from different colonies. J Ornithol 155:801–817. doi: 10.1007/s10336-014-1065-5 CrossRefGoogle Scholar
  51. Sánchez RP, Ciechomski JD (1995) Spawning and nursery grounds of pelagic fish species in the sea-shelf off Argentina and adjacent areas. Sci Mar 59:455–478Google Scholar
  52. Sánchez RP, Remeslo AV, Madirolas A, Ciechomski JD (1995) Distribution and abundance of post-larvae and juveniles of the Patagonian spratt, Sprattus fuegensis, and related hydrographic conditions. Fish Res 23:47–81CrossRefGoogle Scholar
  53. Schiavini A, Yorio P, Gandini P et al (2005) Los pingüinos de las costas argentinas: estado poblacional y conservación. Hornero 20:5–23Google Scholar
  54. Shepard ELC, Wilson RP, Quintana F et al (2008a) Identification of animal movement patterns using tri-axial accelerometry. Endanger Species Res 10:47–60CrossRefGoogle Scholar
  55. Shepard ELC, Wilson RP, Halsey LG et al (2008b) Derivation of body motion via appropriate smoothing of acceleration data. Aquat Biol 4:235–241CrossRefGoogle Scholar
  56. Shepard ELC, Wilson RP, Quintana F et al (2009) Pushed for time or saving fuel: fine-scale energy budgets shed light on currencies in a diving bird. Proc R Soc B 276:3149–3155CrossRefGoogle Scholar
  57. Shepard ELC, Wilson RP, Gómez-Laich A, Quintana F (2010) Buoyed up and slowed down: speed limits for diving birds in shallow water. Aquat Biol 8:259–267CrossRefGoogle Scholar
  58. Simeone A, Wilson RP (2003) In-depth studies of Magellanic penguin (Spheniscus magellanicus) foraging: can we estimate prey consumption by perturbations in the dive profile? Mar Biol 143:825–831CrossRefGoogle Scholar
  59. Skewgar E, Boersma PD, Harris G, Caille G (2007) Anchovy fishery threat to patagonian ecosystem. Science 315:45CrossRefGoogle Scholar
  60. Stearns SC (1977) The evolution of life history traits: a critique of the theory and a review of the data. Ann Rev Ecol Syst 8:145–171CrossRefGoogle Scholar
  61. Suryan RM, Irons DB, Benson J (2000) Prey switching and variable foraging strategies of black-legged kittiwakes and the effect on reproductive success. Condor 102:374–384CrossRefGoogle Scholar
  62. Underwood AJ (1990) Experiments in ecology and their management: their logics, functions, and interpretations. Aust J Ecol 15:365–389CrossRefGoogle Scholar
  63. Underwood AJ (1997) Experiments in ecology. Blackwell, LondonGoogle Scholar
  64. Williams TD (1995) The penguins. Oxford University Press, OxfordGoogle Scholar
  65. Wilson RP (1995) The foraging ecology of penguins. In: Williams T (ed) The penguins. Oxford University Press, Oxford, pp 81–106Google Scholar
  66. Wilson RP (1997) A restraint method for penguins. Mar Ornithol 25:72–73Google Scholar
  67. Wilson RP, Hustler K, Ryan PG et al (1992) Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am Nat 140:179–200CrossRefGoogle Scholar
  68. Wilson RP, Culik BM, Peters G, Bannasch R (1996) Diving behaviour of Gentoo penguins, Pygoscelis papua; factors keeping dive profiles in shape. Mar Biol 126:153–162CrossRefGoogle Scholar
  69. Wilson RP, Pütz K, Peters G et al (1997) Long-term attachment of transmitting and recording devices to penguins and others seabirds. Wildl Soc Bull 25:101–106Google Scholar
  70. Wilson RP, Ropert-Coudert Y, Kato A (2002) Rush and grab strategies in foraging marine endotherms: the case for haste in penguins. Anim Behav 63:85–95CrossRefGoogle Scholar
  71. Wilson RP, Kreye JA, Lucke K, Urquhart H (2004) Antennae on transmitters on penguins: balancing energy budgets on the high wire. J Exp Biol 207:2649–2662CrossRefGoogle Scholar
  72. Wilson RP, Scolaro JA, Gremillet D et al (2005) How do Magellanic penguins cope with variability in their access to prey? Ecol Monogr 75:379–401CrossRefGoogle Scholar
  73. Wilson RP, White CR, Quintana F et al (2006) Moving towards acceleration for estimates of activity-specific metabolic rate in free-living animals: the case of the cormorant. J Anim Ecol 75:1081–1090CrossRefGoogle Scholar
  74. Wilson RP, Shepard ELC, Liebsch N (2008) Prying into the intimate details of animal lives: use of a daily diary on animals. Endanger Species Res 4:123–137CrossRefGoogle Scholar
  75. Wilson RP, Shepard ELC, Quintana F et al (2010) Pedalling downhill and freewheeling up; a penguin perspective on foraging. Aquat Biol 8:193–202CrossRefGoogle Scholar
  76. Wilson RP, McMahon CR, Quintana F et al (2011) N-dimensional animal energetic niches clarify behavioural options in a variable marine environment. J Exp Biol 214:646–656CrossRefGoogle Scholar
  77. Yorio P, Quintana F, Dell’arciprete P, González-Zevallos D (2010) Spatial overlap between foraging seabirds and trawl fisheries: implications for the effectiveness of a marine protected area at Golfo San Jorge, Argentina. Bird Conserv Int 20:320–334CrossRefGoogle Scholar
  78. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle RiverGoogle Scholar
  79. Zimmer I, Ropert-Coudert Y, Kato A et al (2011) Does foraging performance change with age in female Little penguins (Eudyptula minor)? PLoS ONE 6(1):e16098. doi: 10.1371/journal.pone.0016098 CrossRefGoogle Scholar
  80. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Laboratorio de Ecología de Predadores Tope Marinos (LEPTOMA)Centro Nacional Patagónico (CONICET)Puerto MadrynArgentina
  2. 2.Swansea Laboratory for Animal Movement, Biosciences, College of ScienceSwansea UniversitySwanseaUK
  3. 3.Wildlife Conservation SocietyCiudad de Buenos AiresArgentina

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