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Flexible foraging for finding fish: variable diving patterns in Magellanic penguins Spheniscus magellanicus from different colonies

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Abstract

Seabirds have to deal with environmental variability and are predicted to modulate foraging behavior to maximize fitness, with particularly strong selection pressure for optimal behavior during chick provisioning when energy demands are high. We reported data from 42 breeding birds equipped during the early chick-rearing period with depth recorders at four different colonies [Punta Norte (42°S), Bahía Bustamante (45°S), Puerto Deseado (47°S) and Puerto San Julián (49°S)] in patagonian Argentina. Although Magellanic penguins are purported to show little flexibility in foraging behavior, we discovered marked inter-colony differences in diving behavior. Even though the southern marine ecosystems, in general, and the area exploited by Magellanic penguins from the studied colonies, in particular, are usually characterized by their stability, we cannot entirely exclude that interannual differences may have also affected our results. The colonies located in the center of the breeding distribution, Bahía Bustamante and Puerto Deseado, showed the greatest diving and foraging effort with Bahía Bustamante penguins having the deepest and longest dives of all birds and requiring the longest post-dive recovery durations at the surface. Puerto Deseado had the birds with the highest values of diving effort parameters. Penguins from both colonies also had the highest descent and ascent rates during dives. We assume that the clear variation in diving behavior reflects the response of the birds to the varying prey types and availability around the different colonies, but note that, despite this, some colonies fare markedly better than others in breeding.

Zusammenfassung

Flexible Suche nach Fisch: unterschiedliche Tauchmuster von Magellan -Pinguinen Spheniscus magellanicus aus verschiedenen Kolonien

Seevögel müssen Umweltveränderungen bewältigen und können vermutlich ihre Nahrungssuche anpassen, um ihre Fitness zu maximieren, vor allem bei starkem Selektionsdruck für optimales Verhalten während der Jungenaufzucht, wenn der Energiebedarf besonders hoch ist. In vier verschiedenen Kolonien [Punta Norte (42°S), Bahía Bustamante (45°S), Puerto Deseado (47°S) and Puerto San Julián (49°S)] im argentinischen Teil Patagoniens wurden während der frühen Kükenaufzuchtsphase 42 Brutvögel mit Tiefenmessern ausgerüstet. Obwohl Magellan-Pinguine angeblich eine geringe Flexibilität im Nahrungssuchverhalten zeigen, konnten deutliche Unterschiede im Tauchverhalten zwischen den Kolonien festgestellt werden. Wenngleich die südlichen marinen Ökosysteme im Allgemeinen, und das von den untersuchten Magellan-Pinguinen genutzte Gebiet im Speziellen, normalerweise durch ihre Stabilität gekennzeichnet sind, kann nicht gänzlich ausgeschlossen werden, dass Unterschiede zwischen den Jahren die Ergebnisse beeinflusst haben könnten. Die Kolonien, die in der Mitte des Brutverbreitungsgebietes liegen, Bahía Bustamante und Puerto Deseado, zeigten den größten Aufwand für Tauchen und Nahrungssuche. Die Bahía Bustamante Pinguine tauchten von allen Vögeln am tiefsten und am längsten und benötigten die längsten Erholungsphasen an der Wasseroberfläche nach ihren Tauchgängen. Puerto Deseado Pinguine zeigten die höchsten Werte im Tauchaufwand. Vögel aus beiden Kolonien hatten die höchsten Ab- und Auftauchgeschwindigkeiten während der Tauchgänge. Wir nehmen an, dass die Unterschiede im Tauchverhalten die Antwort der Vögel auf variierende Beutetypen und deren Verfügbarkeit um die verschiedenen Kolonien reflektiert. Ungeachtet dessen ist aber darauf hinzuweisen, dass das Brutgeschäft in einigen Kolonien deutlich besser läuft als in anderen.

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References

  • Acha EM, Mianzan HW, Guerrero RA, Favero M, Bava J (2004) Marine fronts at the continental shelves of austral South America: physical and ecological processes. J Mar Syst 44:83–105

    Google Scholar 

  • 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

    Google Scholar 

  • Boersma PD, Rebstock GA (2009) Foraging distance affects reproductive success in Magellanic penguins. Mar Ecol Prog Ser 375:263–275

    Google Scholar 

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

    Google Scholar 

  • Bost CA, Handrich Y, Butler PJ, Fahlman A, Halsey LG, Woakes AJ, Ropert-Coudert Y (2007) Changes in dive profiles as an indicator of feeding success in king and Adélie penguins. Deep Sea Res II 54:248–255

    Google Scholar 

  • Bost CA, Cotté C, Bailleul F, Cherel Y, Charrassin JB, Guinet C, Ainley DG, Weimerskirch H (2009) The importance of oceanographic fronts to marine birds and mammals of the southern oceans. J Mar Syst 78:363–367

    Google Scholar 

  • Butler PJ, Jones DR (1997) The physiology of diving of birds and mammals. Physiol Rev 77:837–899

    CAS  PubMed  Google Scholar 

  • Charrassin JB, Bost CA, Pütz K, Lage J, Dahier T, Zorn T, Le Maho Y (1998) Foraging strategies of incubating and brooding king penguins Aptenodytes patagonicus. Oecologia 114:194–201

    PubMed  Google Scholar 

  • Charrassin JB, Bost CA, Pütz K, Lage J, Dahier T, Le Maho Y (1999) Changes in depth utilization in relation to the breeding stage: a case study with the King Penguin Aptenodytes patagonicus. Mar Ornithol 27:43–47

    Google Scholar 

  • Charrassin JB, Le Maho Y, Bost CA (2002) Seasonal changes in the diving parameters of king penguins (Aptenodytes patagonicus). Mar Biol 141:581–589

    Google Scholar 

  • Chiaradia A, Ropert-Coudert Y, Kato A, Mattern T, Yorke J (2007) Diving behaviour of little penguins from four colonies across their whole distribution range: bathymetry affecting diving effort and fledging success. Mar Biol 151:1535–1542

    Google Scholar 

  • Cook TR, Hamann M, Pichegru L, Bonadonna F, Grémillet D, Ryan PG (2012) GPS and time-depth loggers reveal underwater foraging plasticity in a flying diver, the Cape Cormorant. Mar Biol 159:373–387

    Google Scholar 

  • Crawley MJ (2007) The R book. Wiley, West Sussex

    Google Scholar 

  • Elliott KH, Woo K, Gaston AJ, Benvenuti S, Antonia LD, Davoren GK (2008) Seabird foraging behaviour indicates prey type. Mar Ecol Prog Ser 354:298–303

    Google Scholar 

  • Fauchald P, Erikstad KE (2002) Scale-dependent predator-prey interactions: the aggregative response of seabirds to prey under variable prey abundance and patchiness. Mar Ecol Prog Ser 231:279–291

    Google Scholar 

  • Frere E, Gandini P, Lichtschein V (1996) Variación latitudinal en la dieta del pingüino de magallanes (Spheniscus magellanicus) en la costa Patagónica, Argentina. Ornitol Neotrop 7:35–41

    Google Scholar 

  • Halsey LG, Bost CA, Handrich Y (2007) A thorough and quantified method for classifying seabird diving behaviour. Polar Biol 30:991–1004

    Google Scholar 

  • Hansen JE, Martos P, Madirolas A (2001) Relationship between spatial distribution of the Patagonian stock of Argentine anchovy, Engraulis anchoita, and sea temperatures during late spring to early summer. Fish Oceanogr 10:193–206

    Google Scholar 

  • Härdle W, Simar L (2007) Applied multivariate statistical analysis. Springer, Berlin

    Google Scholar 

  • Harris S, Quintana F, Raya Rey A (2012) Prey search behavior of the Imperial Cormorant (Phalacrocorax atriceps) during the breeding season at Punta León, Argentina. Waterbirds 35:312–323

    Google Scholar 

  • 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

    Google Scholar 

  • Hunt GL (1990) The pelagic distribution of marine birds in a heterogeneous environment. Polar Res 8:43–54. doi:10.1111/j.1751-8369.1990.tb00374.x

    Google Scholar 

  • Kooyman GL (1989) Diverse divers: physiology and behavior. In: Johansen K, Farner DS (eds) Zoophysiology series, vol 23. Springer, Berlin

    Google Scholar 

  • Mahalanobis PC (1948) Historical note on the D3-statistic. Sankhya 9:237–240

    Google Scholar 

  • Márquez F, Robledo J, Escati Peñaloza G, Van der Molen S (2010) Use of different geometric morphometrics tools for the discrimination of phenotypic stocks of the striped clam Ameghinomya antiqua (Veneridae) in north Patagonia, Argentina. Fish Res 101:127–131

    Google Scholar 

  • Morrison ML, Ralph CJ, Verner J, Jehl JR (1990) Avian foraging: theory, methodology, and applications. Stud Avian Biol 13:1–515

    Google Scholar 

  • Parker G, Paterlini MC, Violante RA (1997) El fondo marino. El Mar Argentino y sus Recursos Pesqueros (Tomo 1).In: Boschi EE (ed) INIDEP, Mar del Plata, p 65–87

  • Parkes R, Halsey LG, Woakes AJ, Holder RL, Butler PJ (2002) Oxygen uptake during post dive recovery in a diving bird Aythya fuligula: implications for optimal foraging models. J Exp Biol 205:3945–3954

    PubMed  Google Scholar 

  • Peters G, Wilson RP, Scolaro JA, Laurenti S, Upton J, Galleli H (1998) The diving behavior of Magellanic Penguins at Punta Norte, Península Valdés, Argentina. Colon Waterbirds 21:1–10

    Google Scholar 

  • 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

    Google Scholar 

  • Pichegru L, Ropert-Coudert Y, Kato A, Takahashi A, Dyer BM, Ryan PG (2011) Diving patterns of female macaroni penguins breeding on Marion Island, South Africa. Polar Biol 34:945–954

    Google Scholar 

  • 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

    Google Scholar 

  • Quintana F, Wilson R, Dell´Arciprete P, Shepard E, Gómez-Laich A (2011) Women are from Venus, men from Mars: how may intersex foraging difference be expressed in colonial cormorants? Oikos 120:350–358

    Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Radl A, Culik BM (1999) Foraging behaviour and reproductive success in Magellanic penguins (Spheniscus magellanicus): a comparative study of two colonies in southern Chile. Mar Biol 133:381–393

    Google Scholar 

  • Raya Rey A, 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

    Google Scholar 

  • Raya Rey A, Pütz K, Scioscia G, Lüthi B, Schiavini A (2012) Sexual differences in the foraging behaviour of magellanic penguins related to stage of breeding. Emu 112:90–96

    Google Scholar 

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

    Google Scholar 

  • Ropert-Coudert Y, Kato A, Baudat J, Bost CA, Le Maho Y, Naito Y (2001) Feeding strategies of free-ranging Adélie penguins Pygoscelis adeliae analysed by multiple data recording. Polar Biol 24:460–466

    Google Scholar 

  • 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

    Google Scholar 

  • Ropert-Coudert Y, Kato A, Wilson RP, Cannell B (2006) Foraging strategies and prey encounter rate of free-ranging little penguins. Mar Biol 149:139–148

    Google Scholar 

  • Sabatini ME (2004) Características ambientales, reproducción y alimentación de la merluza (Merluccius hubbsi) y la anchoíta (Engraulis anchoita) en su hábitat reproductivo patagónico. Síntesis y perspectivas. Rev Invest Desarrollo Pesquero 16:5–25

    Google Scholar 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Google Scholar 

  • Sánchez RP, Remeslo A, Madirolas A, Dechiechomski JD (1995) Distribution and abundance of post-larvae and juveniles of the Patagonian sprat, Sprattus fuegensis, and related hydrographic conditions. Fish Res 23:47–81

    Google Scholar 

  • Schiavini A, Yorio P, Gandini P, Raya Rey A, Boersma PD (2005) Los pingüinos de las costas argentinas: estado poblacional y conservación. Hornero 20:5–23

    Google Scholar 

  • Scolaro JA, Wilson RP, Laurenti S, Kierspel M, Gallelli H, Upton J (1999) Feeding preferences of the magellanic penguin over its breeding range in Argentina. Waterbirds 22:104–110

    Google Scholar 

  • Shepard ELC, Wilson RP, Quintana F, Gómez-Laich A, Forman DW (2009) Pushed for time or saving on fuel: fine-scale energy budgets shed light on currencies in a diving bird. Proc R Soc Lond B 276:3149–3155

    Google Scholar 

  • Simeone A, Luna-Jorquera G, Bernal M, Garthe S, Sepúlveda F, Villablanca R, Ellenberg U, Contreras M, Muñoz J, Ponce T (2003) Breeding distribution and abundance of seabirds on islands off north-central Chile. Rev Chil Hist Nat 76:323–333

    Google Scholar 

  • 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

    Google Scholar 

  • Takahashi A, Dunn MJ, Trathan PN, Sato K, Naito Y, Croxall JP (2003) Foraging strategies of Chinstrap Penguins at Signy Island, Antarctica: importance of benthic feeding on Antarctic krill. Mar Ecol Prog Ser 250:279–289

    Google Scholar 

  • Tremblay Y, Cherel Y (2000) Benthic and pelagic dives: a new foraging behaviour in rockhopper penguins. Mar Ecol Prog Ser 204:257–267

    Google Scholar 

  • Valdano SG, Di Rienzo J (2008) Discovering meaningful groups in hierarchical cluster analysis. An extension to the multivariate case of a multiple comparison method based on cluster analysis. InterStat. Available from http://interstat.statjournals.net/YEAR/2007/abstracts/0704002.php?Name=704002

  • Walker BG, Boersma PD (2003) Diving behavior of magellanic penguins (Spheniscus magellanicus) at Punta Tombo, Argentina. Can J Zool 81:1471–1483

    Google Scholar 

  • Walton P, Ruxton GD, Monagham P (1998) Avian diving, respiratory physiology and the marginal value theorem. Anim Behav 56:165–174

    CAS  PubMed  Google Scholar 

  • Watanuki Y, Kato A, Mori Y, Naito Y (1993) Diving performance of Adélie penguins in relation to food availability in fast sea-ice areas: comparison between years. J Anim Ecol 62:634–646

    Google Scholar 

  • Watanuki Y, Kato A, Naito Y, Robertson G, Robinson S (1997) Diving and foraging behaviour of Adélie penguins in areas with and without fast sea ice. Polar Biol 17:296–304

    Google Scholar 

  • Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Sea Res II 54:211–223

    Google Scholar 

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

    Google Scholar 

  • Wilson RP (2003) Penguins predict their performance. Mar Ecol Prog Ser 249:305–310

    Google Scholar 

  • Wilson RP, Hustler K, Ryan PG, Burger AE, Noldeke EC (1992) Diving birds in cold water: do Archimedes and Boyle determine energetic costs? Am Nat 140:179–200

    Google Scholar 

  • Wilson RP, Pütz K, Bost CA, Culik BM, Bannasch R, Reins T, Adelung D (1993) Diel dive depth in penguins in relation to diel vertical migration of prey: whose dinner by candlelight? Mar Ecol Prog Ser 94:101–104

    Google Scholar 

  • Wilson RP, Pütz K, Grémillet D, Culik BM, Kierspel M, Regel J, Bost CA, Lage J, Cooper J (1995) Reliability of stomach temperature changes in determining feeding characteristics of seabirds. J Exp Biol 198:1115–1135

    CAS  PubMed  Google Scholar 

  • Wilson RP, Wilson MP (1995) The foraging behaviour of the African Penguin. In: Dann P, Norman I, Reilly P (eds) The penguins: ecology and management. Surrey Beatty, Sidney, pp 244–265

    Google Scholar 

  • 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

    Google Scholar 

  • Wilson RP, Bost CA, Pütz K, Charrassin JB, Culik BM, Adelung D (1997) Southern rockhopper penguin Eudyptes chrysocome chrysocome foraging at Possession Island. Polar Biol 17:323–329

    CAS  Google Scholar 

  • Wilson RP, Scolaro JA, Grémillet D, Kierspel M, Laurenti S, Upton J, Gallelli H, Quintana F, Frere E, Müller G, Thor Straten M, Zimmer I (2005) How do magellanic penguins cope with variability in their access to prey? Ecol Monogr 75:379–401

    Google Scholar 

  • 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

    Google Scholar 

  • Wilson RP, Shepard ELC, Gómez-Laich A, Frere E, Quintana F (2010) Pedalling downhill and freewheeling up; a penguin perspective on foraging. Aquat Biol 8:193–202

    Google Scholar 

  • Wilson RP, McMahon CR, Quintana F, Frere E, Scolaro JA, Hays GC, Bradshaw CJA (2011) N-dimensional animal energetic niches clarify behavioural options in a variable marine environment. J Exp Biol 214:646–656

    PubMed  Google Scholar 

  • Ydenberg RC, Clark CW (1989) Aerobiosis and anaerobiosis during diving by western grebes: an optimal foraging approach. J Theor Biol 139:437–449

    Google Scholar 

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

    Google Scholar 

  • Zimmer I, Wilson RP, Beaulieu M, Ropert-Coudert Y, Kato A, Ancel A, Plötz J (2010) Dive efficiency versus depth in foraging emperor penguins. Aquat Biol 8:269–277

    Google Scholar 

  • Zimmer I, Ropert-Coudert Y, Poulin N, Kato A, Chiaradia A (2011a) Evaluating the relative importance of intrinsic and extrinsic factors on the foraging activity of top predators: a case study on female little penguins. Mar Biol 158:715–722

    Google Scholar 

  • Zimmer I, Ropert-Coudert Y, Kato A, Ancel A, Chiaradia A (2011b) Does foraging performance change with age in female little penguins (Eudyptula minor)? PLoS ONE 6(1):e16098. doi:10.1371/journal.pone.0016098

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New York

    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 F.Q. and by a Rolex Award for Enterprise awarded to R.P.W. 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 two anonymous reviewers who provided valuable comments and contributed to a significant improvement of this paper. This work is dedicated to the memory of Néstor C. Kirchner (1950–2010), former President of Argentina, who revitalized and promoted the scientific Argentinean system, and to his wife, the current President, Cristina Fernández de Kirchner, who continues his legacy.

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Correspondence to Juan E. Sala.

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J. E. Sala, R. P. Wilson, E. Frere and F. Quintana contributed equally to the work.

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Sala, J.E., Wilson, R.P., Frere, E. et al. Flexible foraging for finding fish: variable diving patterns in Magellanic penguins Spheniscus magellanicus from different colonies. J Ornithol 155, 801–817 (2014). https://doi.org/10.1007/s10336-014-1065-5

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