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Behavioural adjustments during foraging in two diving seabirds: king and macaroni penguins

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Abstract

Optimal foraging theory predicts that diving predators should maximise their energy intake while minimizing the costs of their foraging activities at depth. This hypothesis was tested in two breath-hold divers that foraged in the pelagic waters off Kerguelen Island, southern Indian Ocean. Macaroni penguins (Eudyptes chrysolophus) feed predominately on crustaceans at moderate depths (ca. 50 m), while king penguins (Aptenodytes patagonicus) feed on mesopelagic fish at deep depths (ca. 100–150 m). We instrumented 22 penguins with time-depth recorders during the breeding season of the 2014 southern summer, just before they went to sea. Birds were recaptured after one to five foraging trips and the dive data were analysed on the level of single dive cycles and entire dive bouts. Both species adjusted their diving behaviour and modulated their foraging activity in accordance with their experience in their previous dives. Foraging activity during a dive (in terms of number of wiggles per dive) was greater if birds targeted the same depth as the previous dive. The penguins spent less time at the surface between two prey capture attempt dives than when a prey capture attempt dive was preceded by a non-prey capture attempt dive. Dive bout analyses showed that foraging activity increased with bout duration, while transit time during dives decreased with bout duration. Our findings are in general agreement with predictions based on optimal foraging models. The results suggest that penguins anticipated the depth of their next dive based on their encounter of a prey patch in the previous dive and optimized their chances of feeding success by spending minimal time at the surface and in transit to the patch depth. Once penguins detected a prey patch, these behavioural adjustments allowed them to rapidly return to that patch, increasing their chances of feeding again before the prey disperses.

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Data availability

The datasets used for this study are available from the corresponding author on reasonable request.

References

  • Bannasch R, Wilson R, Culik B (1994) Hydrodynamic aspects of design and attachment of a back-mounted device in penguins. J Exp Biol 194:83

    Google Scholar 

  • Benoit-Bird KJ, Battaile BC, Heppell SA, Hoover B, Irons D, Jones N, Kuletz KJ, Nordstrom CA, Paredes R, Suryan RM, Waluk CM, Trites AW (2013) Prey patch patterns predict habitat use by top marine predators with diverse foraging strategies. PLoS ONE 8:e53348. https://doi.org/10.1371/journal.pone.0053348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bocher P, Cherel Y, Labat J-P, Mayzaud P, Razouls S, Jouventin P (2001) Amphipod-based food web: Themisto gaudichaudii caught in nets and by seabirds in Kerguelen waters, southern Indian Ocean. Mar Ecol Prog Ser 223:261–276

    Article  Google Scholar 

  • Bost CA, Koubbi P, Genevois F, Ruchon L, Ridoux V (1994) Gentoo penguin Pygoscelis papua diet as an indicator of planktonic availability in the Kerguelen Islands. Polar Biol 14:147–153

    Article  Google Scholar 

  • Bost CA, Zorn T, Le Maho Y, Duhamel G (2002) Feeding of diving predators and diel vertical migration of prey: king penguins’ diet versus trawl sampling at Kerguelen Islands. Mar Ecol Prog Ser 227:51–61

    Article  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 Part II Top Stud Oceanogr 54:248–255. https://doi.org/10.1016/j.dsr2.2006.11.007

    Article  Google Scholar 

  • Boyd IL (1996) Temporal scales of foraging in a marine predator. Ecology 77:426–434

    Article  Google Scholar 

  • Boyd IL (1997) The behavioural and physiological ecology of diving. TREE 12:213–217

    CAS  PubMed  Google Scholar 

  • Butler PJ (2001) Diving beyond the limits. Physiology 16:222–227

    Article  CAS  Google Scholar 

  • Butler PJ (2004) Metabolic regulation in diving birds and mammals. Respir Physiol Neurobiol 141:297–315

    Article  Google Scholar 

  • Butler PJ, Jones DR (1997) Physiology of diving of birds and mammals. Physiol Rev 77:837–898

    Article  CAS  Google Scholar 

  • Carroll G, Slip D, Jonsen I, Harcourt R (2014) Supervised accelerometry analysis can identify prey capture by penguins at sea. J Exp Biol 217:4295–4302. https://doi.org/10.1242/jeb.113076

    Article  PubMed  Google Scholar 

  • Carroll G, Harcourt R, Pitcher BJ, Slip D, Jonsen I (2018) Recent prey capture experience and dynamic habitat quality mediate short-term foraging site fidelity in a seabird. Proc R Soc B Biol Sci 285:20180788. https://doi.org/10.1098/rspb.2018.0788

    Article  Google Scholar 

  • Catul V, Gauns M, Karuppasamy PK (2011) A review on mesopelagic fishes belonging to family Myctophidae. Rev Fish Biol Fish 21:339–354. https://doi.org/10.1007/s11160-010-9176-4

    Article  Google Scholar 

  • Charrassin JB, Bost C-A (2001) Utilisation of the oceanic habitat by king penguins over the annual cycle. Mar Ecol Prog Ser 221:285–298

    Article  Google Scholar 

  • Charrassin JB, Maho YL, Bost C-A (2002) Seasonal changes in the diving parameters of king penguins (Aptenodytes patagonicus). Mar Biol 141:581–589. https://doi.org/10.1007/s00227-002-0843-4

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Guinet C, Vanpe C (2007) Stable isotopes document seasonal changes in trophic niches and winter foraging individual specialization in diving predators from the Southern Ocean. J Anim Ecol 76:826–836. https://doi.org/10.1111/j.1365-2656.2007.01238.x

    Article  PubMed  Google Scholar 

  • Collins MA, Xavier JC, Johnston NM, North AW, Enderlein P, Tarling GA, Waluda CM, Hawker EJ, Cunningham NJ (2008) Patterns in the distribution of myctophid fish in the northern Scotia Sea ecosystem. Polar Biol 31:837–851. https://doi.org/10.1007/s00300-008-0423-2

    Article  Google Scholar 

  • Cornick LA, Inglis SD, Willis K, Horning M (2006) Effects of increased swimming costs on foraging behavior and efficiency of captive Steller sea lions: evidence for behavioral plasticity in the recovery phase of dives. J Exp Mar Biol Ecol 333:306–314

    Article  Google Scholar 

  • Culik BM, Pütz K, Wilson RP, Allers D, Lage J, Bost CA, Le Maho Y (1996) Diving energetics in king penguins (Aptenodytes patagonicus). J Exp Biol 199:973–983

    CAS  PubMed  Google Scholar 

  • Duhamel G, Koubbi P, Ravier C (2000) Day and night mesopelagic fish assemblages off the Kerguelen Islands (Southern Ocean). Polar Biol 23:106–112

    Article  Google Scholar 

  • Elliott KH, Davoren GK, Gaston AJ (2008) Increasing energy expenditure for a deep-diving bird alters time allocation during the dive cycle. Anim Behav 75:1311–1317. https://doi.org/10.1016/j.anbehav.2007.10.026

    Article  Google Scholar 

  • Fahlman A, Svärd C, Rosen DA, Jones DR, Trites AW (2008) Metabolic costs of foraging and the management of O2 and CO2 stores in Steller sea lions. J Exp Biol 211:3573–3580

    Article  Google Scholar 

  • Glen F, Broderick AC, Godley BJ, Metcalfe JD, Hays GC (2001) Dive angles for a green turtle (Chelonia mydas). J Mar Biol Assoc U K 81:683–686

    Article  Google Scholar 

  • Green JA (2003) Energetics of diving in macaroni penguins. J Exp Biol 206:43–57. https://doi.org/10.1242/jeb.00059

    Article  CAS  PubMed  Google Scholar 

  • Guinet C, Cherel Y, Ridoux V, Jouventin P (1996) Consumption of marine resources by seabirds and seals in Crozet and Kerguelen waters: changes in relation to consumer biomass 1962–85. Antarct Sci 8:23–30

    Article  Google Scholar 

  • Halsey LG, Butler PJ, Blackburn TM (2006) A phylogenetic analysis of the allometry of diving. Am Nat 167:276–287

    Article  Google Scholar 

  • Halsey LG, Bost C-A, Handrich Y (2007) A thorough and quantified method for classifying seabird diving behaviour. Polar Biol 30:991–1004. https://doi.org/10.1007/s00300-007-0257-3

    Article  Google Scholar 

  • Handrich Y, Bevan RM, Charrassin JB, Pütz K, Woakes AJ, Le Maho Y (1997) Hypothermia in foraging king penguins. Nature 388:64–67

    Article  CAS  Google Scholar 

  • Hanuise N, Bost C-A, Handrich Y (2013) Optimization of transit strategies while diving in foraging king penguins: Optimization of transit in diving king penguins. J Zool 290:181–191. https://doi.org/10.1111/jzo.12026

    Article  Google Scholar 

  • Harcourt RG, Bradshaw CJ, Dickson K, Davis LS (2002) Foraging ecology of a generalist predator, the female New Zealand fur seal. Mar Ecol Prog Ser 227:11–24

    Article  Google Scholar 

  • Hayden BY, Pearson JM, Platt ML (2011) Neuronal basis of sequential foraging decisions in a patchy environment. Nat Neurosci 14:933–939. https://doi.org/10.1038/nn.2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Houston AI, Carbone C (1992) The optimal allocation of time during the diving cycle. Behav Ecol 3:255–265

    Article  Google Scholar 

  • Hunt GL (1990) The pelagic distribution of marine birds in a heterogeneous environment. Polar Res 8:43–54

    Article  Google Scholar 

  • Kaartvedt S, Staby A, Aksnes D (2012) Efficient trawl avoidance by mesopelagic fishes causes large underestimation of their biomass. Mar Ecol Prog Ser 456:1–6. https://doi.org/10.3354/meps09785

    Article  Google Scholar 

  • Kooyman GL (1989) Diverse Divers. Springer, Berlin

    Book  Google Scholar 

  • Kramer DL (1988) The behavioral ecology of air breathing by aquatic animals. Can J Zool 66:89–94

    Article  Google Scholar 

  • Le Boeuf BJ, Crocker DE, Grayson J, Gedamke J, Webb PM, Blackwell SB, Costa DP (2000) Respiration and heart rate at the surface between dives in northern elephant seals. J Exp Biol 203:3265–3274

    PubMed  Google Scholar 

  • Mori Y (1998) The optimal patch use in divers: optimal time budget and the number of dive cycles during bout. J Theor Biol 190:187–199

    Article  Google Scholar 

  • Mori Y, Takahashi A, Mehlum F, Watanuki Y (2002) An application of optimal diving models to diving behaviour of Brünnich’s guillemots. Anim Behav 64:739–745. https://doi.org/10.1006/anbe.2002.3093

    Article  Google Scholar 

  • Ponganis PJ, Kooyman GL (2000) Diving physiology of birds: a history of studies on polar species. Comp Biochem Physiol A Mol Integr Physiol 126:143–151

    Article  CAS  Google Scholar 

  • Ponganis PJ, Kooyman GL, Van Dam R, LeMaho Y (1999) Physiological responses of king penguins during simulated diving to 136 m depth. J Exp Biol 202:2819–2822

    PubMed  Google Scholar 

  • Ropert-Coudert Y, Grémillet D, Kato A, Ryan PG, Naito Y, Le Maho Y (2004) A fine-scale time budget of Cape gannets provides insights into the foraging strategies of coastal seabirds. Anim Behav 67:985–992. https://doi.org/10.1016/j.anbehav.2003.09.010

    Article  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. https://doi.org/10.1007/s00227-005-0188-x

    Article  Google Scholar 

  • Sato K (2004) Why do macaroni penguins choose shallow body angles that result in longer descent and ascent durations? J Exp Biol 207:4057–4065. https://doi.org/10.1242/jeb.01265

    Article  PubMed  Google Scholar 

  • Sato K, Naito Y, Kato A, Niizuma Y, Watanuki Y, Charrassin JB, Bost C-A, Handrich Y, Le Maho Y (2002) Buoyancy and maximal diving depth in penguins. J Exp Biol 205:1189–1197

    PubMed  Google Scholar 

  • Saunders RA, Fielding S, Thorpe SE, Tarling GA (2013) School characteristics of mesopelagic fish at South Georgia. Deep Sea Res Part Oceanogr Res Pap 81:62–77. https://doi.org/10.1016/j.dsr.2013.07.007

    Article  Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • Thompson D, Fedak MA (2001) How long should a dive last? A simple model of foraging decisions by breath-hold divers in a patchy environment. Anim Behav 61:287–296. https://doi.org/10.1006/anbe.2000.1539

    Article  Google Scholar 

  • Thums M, Bradshaw CJA, Sumner MD, Horsburgh JM, Hindell MA (2013) Depletion of deep marine food patches forces divers to give up early. J Anim Ecol 82:72–83. https://doi.org/10.1111/j.1365-2656.2012.02021.x

    Article  PubMed  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

    Article  Google Scholar 

  • Wakefield E, Phillips R, Matthiopoulos J (2009) Quantifying habitat use and preferences of pelagic seabirds using individual movement data: a review. Mar Ecol Prog Ser 391:165–182. https://doi.org/10.3354/meps08203

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Watanuki Y, Burger AE (1999) Body mass and dive duration in alcids and penguins. Can J Zool 77:1838–1842

    Article  Google Scholar 

  • Weimerskirch H (2007) Are seabirds foraging for unpredictable resources? Deep Sea Res Part II Top Stud Oceanogr 54:211–223. https://doi.org/10.1016/j.dsr2.2006.11.013

    Article  Google Scholar 

  • Weimerskirch H, Bertrand S, Silva J, Bost C, Peraltilla S (2012) Foraging in Guanay cormorant and Peruvian booby, the major guano-producing seabirds in the Humboldt Current System. Mar Ecol Prog Ser 458:231–245. https://doi.org/10.3354/meps09752

    Article  Google Scholar 

  • Wilson R, Wilson M (1995) The foraging behaviour of the African penguin Spheniscus demersus. In: The penguins: ecology and management. Dann P, Norman, I, Reilly P pp 244–265

  • Wilson RP (1995) Foraging ecology. In: The penguins, Oxford University Press. Williams TD, Oxford, pp 81–106

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wilson RP, Quintana F (2004) Surface pauses in relation to dive duration in imperial cormorants; how much time for a breather? J Exp Biol 207:1789–1796. https://doi.org/10.1242/jeb.00967

    Article  PubMed  Google Scholar 

  • Ydenberg RC, Forbes LS (1988) Diving and foraging in the western grebe. Ornis Scand 129–133

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Acknowledgements

The authors thank all the fieldworkers for their help with data collection in the Kerguelen area, especially Florian Orgeret, Elie Gajet and Alexandre Corbeau. The study was supported financially and logistically by the Institut Polaire Français Paul Emile Victor (program no. 394 “Oiseaux Plongeurs”, C.A. Bost) and the Terres Australes et Antarctiques Françaises. The ethics committee of Institut polaire français Paul Emile Victor approved all field procedures. We are especially indebted to Manfred Enstipp and Carin Reisinger for helpful comments and English editing.

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Charles-André Bost contributed to the study conception and design. Analysis was performed by Eugénie Tessier. The first draft of the manuscript was written by Eugénie Tessier and Charles-André Bost commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Eugénie Tessier.

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All experimental procedures were approved by the French ethics committee and the French Polar Environmental Committee and conducted in accordance with their guidelines.

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Tessier, E., Bost, CA. Behavioural adjustments during foraging in two diving seabirds: king and macaroni penguins. Mar Biol 167, 138 (2020). https://doi.org/10.1007/s00227-020-03711-z

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