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

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.

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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 44:83–105

    Article  Google 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 40:279–288

    Article  Google 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 194:83–96

    Google 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 375:263–275

    Article  Google Scholar 

  6. Boersma PD, Rebstock GA, Frere E, Moore SE (2009) Following the fish: penguins and productivity in the South Atlantic. Ecol Monogr 79:59–76

    Article  Google 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 54:248–255

    Article  Google Scholar 

  8. Boswall J, MacIver D (1975) The Magellanic penguin Spheniscus magellanicus. In: Stonehouse B (ed) The biology of penguins. Macmillan, London, pp 271–305

    Google Scholar 

  9. Brown JH, Gilloly JF, Allen AP et al (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789

    Article  Google Scholar 

  10. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  11. Crawley MJ (2007) The R Book. Wiley, West Sussex

    Book  Google 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 83:3466–3475

    Article  Google Scholar 

  13. Gandini PA, Frere E, Pettovello AD, Cedrola PV (1999) Interaction between Magellanic penguins and shrimp fisheries in Patagonia, Argentina. Condor 101:783–789

    Article  Google 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 2:23–33

    Article  Google Scholar 

  15. Gómez-Laich A, Wilson RP, Quintana F, Shepard ELC (2008) Identification of imperial cormorant Phalacrocorax atriceps behaviour using accelerometers. Endanger Species Res 10:29–37

    Article  Google 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 399:151–155

    Article  Google 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 160:1697–1707

    Article  Google 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 212:471–482

    Article  CAS  Google 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

    Article  Google 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 319:15–25

    Article  Google Scholar 

  21. Halsey L (2011) The challenge of measuring energy expenditure: current field and laboratory methods. Comp Biochem Physiol Part A 158:247–251

    Article  Google Scholar 

  22. Halsey L, Woakes A, Butler P (2003) Testing optimal foraging models for air-breathing divers. Anim Behav 65:641–653

    Article  Google 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 152:197–202

    Article  CAS  Google 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 82:396–404

    Article  CAS  Google 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 213:3874–3880

    Article  Google 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 35:312–323

    Article  Google Scholar 

  27. Hennicke JC, Culik BM (2005) Foraging performance and reproductive success of Humboldt penguins in relation to prey availability. Mar Ecol Prog Ser 296:173–181

    Article  Google 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 35:623–630

    Article  Google Scholar 

  29. Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819

    Article  CAS  Google 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 147:606–614

    Article  Google 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 17:93–121

    Article  Google Scholar 

  32. Luna-Jorquera G, Culik BM (1999) Diving behaviour of Humboldt Penguins Spheniscus humboldti in northern Chile. Mar Ornithol 27:67–76

    Google Scholar 

  33. Luna-Jorquera G, Culik BM (2000) Metabolic rates of swimming Humboldt penguins. Mar Ecol Prog Ser 203:301–309

    Article  CAS  Google 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 154–177

    Google 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 269-287

  36. Peters G, Wilson RP, Scolaro JA et al (1998) The diving behavior of Magellanic Penguins at Punta Norte, Península Valdés, Argentina. Waterbirds 21:1–10

    Article  Google 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 148:14–26

    Article  Google 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

    Article  CAS  Google Scholar 

  39. Pyke GH (1984) Optimal foraging theory: a critical review. A Rev Ecol Syst 15:523–575

    Article  Google 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

    Article  CAS  Google 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 157:515–525

    Article  Google 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 120:350–358

    Article  Google Scholar 

  43. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google 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 151:933–943

    Article  Google 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 112:90–96

    Article  Google Scholar 

  46. Rivas AL, Dogliotti AI, Gagliardini DA (2006) Seasonal variability in satellite-measured surface chlorophyll in the Patagonian Shelf. Cont Shelf Res 26:703–720

    Article  Google 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 15:824–830

    Article  Google 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

    Article  CAS  Google 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

    Article  Google 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

    Article  Google 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 59:455–478

    Google 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 23:47–81

    Article  Google Scholar 

  53. Schiavini A, Yorio P, Gandini P et al (2005) Los pingüinos de las costas argentinas: estado poblacional y conservación. Hornero 20:5–23

    Google Scholar 

  54. Shepard ELC, Wilson RP, Quintana F et al (2008a) Identification of animal movement patterns using tri-axial accelerometry. Endanger Species Res 10:47–60

    Article  Google Scholar 

  55. Shepard ELC, Wilson RP, Halsey LG et al (2008b) Derivation of body motion via appropriate smoothing of acceleration data. Aquat Biol 4:235–241

    Article  Google 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 276:3149–3155

    Article  Google 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 8:259–267

    Article  Google 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 143:825–831

    Article  Google Scholar 

  59. Skewgar E, Boersma PD, Harris G, Caille G (2007) Anchovy fishery threat to patagonian ecosystem. Science 315:45

    Article  CAS  Google 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 8:145–171

    Article  Google 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 102:374–384

    Article  Google Scholar 

  62. Underwood AJ (1990) Experiments in ecology and their management: their logics, functions, and interpretations. Aust J Ecol 15:365–389

    Article  Google Scholar 

  63. Underwood AJ (1997) Experiments in ecology. Blackwell, London

    Google Scholar 

  64. Williams TD (1995) The penguins. Oxford University Press, Oxford

    Google Scholar 

  65. Wilson RP (1995) The foraging ecology of penguins. In: Williams T (ed) The penguins. Oxford University Press, Oxford, pp 81–106

    Google Scholar 

  66. Wilson RP (1997) A restraint method for penguins. Mar Ornithol 25:72–73

    Google 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 140:179–200

    Article  Google 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 126:153–162

    Article  Google 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 25:101–106

    Google 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 63:85–95

    Article  Google 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 207:2649–2662

    Article  Google 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 75:379–401

    Article  Google 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 75:1081–1090

    Article  Google 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 4:123–137

    Article  Google Scholar 

  75. Wilson RP, Shepard ELC, Quintana F et al (2010) Pedalling downhill and freewheeling up; a penguin perspective on foraging. Aquat Biol 8:193–202

    Article  Google 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 214:646–656

    Article  Google 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 20:320–334

    Article  Google Scholar 

  78. Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

    Google 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

    Article  CAS  Google Scholar 

  80. Zuur AF, Ieno EN, Walker NJ et al (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    Book  Google Scholar 

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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.

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Correspondence to J. E. Sala.

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Communicated by S. Garthe.

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Sala, J.E., Wilson, R.P. & Quintana, F. Foraging effort in Magellanic penguins: balancing the energy books for survival?. Mar Biol 162, 501–514 (2015). https://doi.org/10.1007/s00227-014-2581-9

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Keywords

  • Total Energy Expenditure
  • Daily Diary
  • Bottom Phase
  • Metabolic Power
  • Estimate Energy Expenditure