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Flexible foraging strategies in a diving seabird with high flight cost

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Abstract

How central-place foragers change search strategy in response to environmental conditions is poorly known. Foragers may vary the total distance travelled and how far they range from the central place in response to variation in the distribution of their prey. One potential reason as to why they would extend the length of their foraging trip and its distance from the colony would be to increase prey quality or quantity, despite incurring higher transit costs. To test this trade-off hypothesis in a species with high flight costs, we recorded the foraging behaviour of razorbills (Alca torca) using state-of-the-art techniques that log both individual horizontal (flight activity) and vertical (dive activity) movements. We show that the distance that razorbills travelled to foraging locations increased with sea-surface temperature, which may relate to higher prey quality or quantity. This relation is supported by an indirect index of patch quality, based on dive profiles, which also increased with travel distance from the colony. Furthermore, we show that this index was highest during the daily peak in diving activity, around midday. Taken together, these results suggest that razorbills are capable of adjusting their search strategies sensitively in response to proximate environmental cues.

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References

  • Alonso JA, Alonso JC, Carrascal LM, Munozpulido R (1994) Flock size and foraging decisions in central place foraging White Storks Ciconia Ciconia. Behaviour 129:279–292

    Article  Google Scholar 

  • Ashmole NP (1963) The regulation of numbers of tropical oceanic birds. Ibis 103b:458–473

    Article  Google Scholar 

  • Baird PH (1991) Optimal foraging and intraspecific competition in the tufted puffin. Condor 93:503–515

    Article  Google Scholar 

  • Birt VL, Birt TP, Goulet D, Cairns DK, Montevecchi WA (1987) Ashmole’s halo: Direct evidence for prey depletion by a seabird. Mar Ecol Prog Ser 40:205–208

    Article  Google Scholar 

  • Burger AE, Powell DW (1990) Diving depths and diet of Cassin’s Auklet at Reef Island, British Columbia. Can J Zool 68:1572–1577

    Article  Google Scholar 

  • Chapdelaine G, Brousseau P (1996) Diet of Razorbill Alca torda chicks and breeding success in St. Mary’s Island, Gulf of St. Lawrence, Quebec, Canada, 1990–1992. In: Montevecchi WA (ed) Studies of high-latitude seabirds 4 Trophic relationships and energetics of endotherms in cold ocean systems. Environment Canada. Canadian Wildlife Service, Canada, pp 27–36

    Google Scholar 

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

    Book  Google Scholar 

  • Cuthill I, Kacelnik A (1990) Central place foraging: a re-appraisal of the “loading effect”. Anim Behav 40:1087–1101

    Article  Google Scholar 

  • Dean B (2012) The at-sea behaviour of the Manx Shearwater. Zoology. University of Oxford, Oxford

    Google Scholar 

  • Decker MB, Hunt GL (1996) Foraging by murres (Uria spp) at tidal fronts surrounding the Pribilof islands, Alaska, USA. Mar Ecol Prog Ser 139:1–10

    Article  Google Scholar 

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

    Google Scholar 

  • Duffy DC (1983) The foraging ecology of Peruvian seabirds. Auk 100:800–810

    Google Scholar 

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

    Article  Google Scholar 

  • Elliott KH, Davoren GK, Gaston AJ (2008b) Time allocation by a deep-diving bird reflects prey type and energy gain. Anim Behav 75:1301–1310

    Article  Google Scholar 

  • Elliott KH, Woo KJ, Gaston AJ, Benvenuti S, Dall’Antonia L, Davoren GK (2009) Central-place foraging in an Arctic seabird provides evidence for storer-Ashmole’s halo. Auk 126:613–625

    Article  Google Scholar 

  • Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behavior by a monomorphic seabird represents risk partitioning. Behav Ecol 21(5):1024–1032

    Article  Google Scholar 

  • Elliott KH, Ricklefs RE, Gaston AJ, Hatch SA, Speakman JR, Davoren GK (2013) High flight costs, but low dive costs, in auks support the biomechanical hypothesis for flightlessness in penguins. Proc Natl Acad Sci 110:9380–9384

    Article  CAS  Google Scholar 

  • Frey-roos F, Brodmann PA, Reyer HU (1995) Relationships between food resources, foraging patterns, and reproductive success in the water pipit, Anthus sp. spinoletta. Behav Ecol 6:287–295

    Article  Google Scholar 

  • Gaston AJ (1985) Energy invested in reproduction by thick-billed murres (Uria lomvia). Auk 102:447–458

    Google Scholar 

  • Gaston AJ (2004) Seabirds: a natural history. Yale University Press, New Haven

    Google Scholar 

  • Gaston AJ, Ydenberg RC, Smith GEJ (2007) Ashmole’s halo and population regulation in seabirds. Mar Ornithol 35:119–126

    Google Scholar 

  • Gaston AJ, Elliott KH, Ropert-Coudert Y, Kato A, MacDonald C, Mallory ML (2013) Modeling foraging range for breeding colonies of thick-billed murres Uria lomvia in the eastern Canadian Arctic and potential overlap with industrial development. Biol Conserv 168:134–143

    Article  Google Scholar 

  • Grémillet D (1997) Catch per unit effort, foraging efficiency, and parental investment in breeding great cormorants (Phalacrocorax carbo carbo). ICES J Mar Sci 54:635–644

    Article  Google Scholar 

  • Guilford TC, Meade J, Freeman R, Biro D, Evans T, Bonadonna F, Boyle D, Roberts S, Perrins CM (2008) GPS tracking of the foraging movements of Manx Shearwaters Puffinus puffinus breeding on Skomer Island, Wales. Ibis 150:462–473

    Article  Google Scholar 

  • Haney JC, Schauer AES (1994) Environmental variability facilitates coexistence within an alcid community at sea. Mar Ecol Prog Ser 103:221–237

    Article  Google Scholar 

  • Hansen ES, Ricklefs RE (2004) Foraging by deep-diving birds is not constrained by an aerobic diving limit: a model of avian depth-dependent diving metabolic rate. Am Nat 163:358–374

    Article  Google Scholar 

  • Harris MP, Wanless S (1986) The food of young Razorbills on the Isle of May and a comparison with that of young Guillemots and Puffins. Ornis Scand 17:41–46

    Article  Google Scholar 

  • Hipfner JM, Chapdelaine G (2002) Razorbill (Alca torca). The Birds of North America Inc, Philadelphia

    Google Scholar 

  • Hofmann EE, Murphy EJ (2004) Advection, krill, and Antarctic marine ecosystems. Antarct Sci 16:487–499

    Article  Google Scholar 

  • Houston AI, McNamara JM (1985) A general theory of central place foraging for single-prey loaders. Theor Popul Biol 28:233–262

    Article  Google Scholar 

  • Hunt GLJ, Schneider DC (1987) Scale-dependent processes in the physical and biological environment of marine birds. In: CJ P (ed) Seabirds: feeding biology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 7–42

    Google Scholar 

  • Hunt GL, Heinemann D, Everson I (1992) Distributions and predator-prey interactions of macaroni penguins, Antarctic fur seals, and. Antarctic krill near Bird Island, South Georgia. Mar Ecol Prog Ser 86:15–30

    Article  Google Scholar 

  • Irons DB (1998) Foraging area fidelity of individual seabirds in relation to tidal cycles and flock feeding. Ecology 79:647–655

    Article  Google Scholar 

  • Jenkins SH (1980) A size-distance relation in food selection by beavers. Ecology 61:740–746

    Article  Google Scholar 

  • Jodice PGR, Collopy MW (1999) Diving and foraging patterns of Marbled Murrelets (Brachyramphus marmoratus): testing predictions from optimal-breathing models. Can J Zool Revue Canadienne De Zoologie 77:1409–1418

    Article  Google Scholar 

  • Kooyman GL, Ponganis PJ (1998) The physiological basis of diving to depth: birds and mammals. Annu Rev Physiol 60:19–32

    Article  CAS  Google Scholar 

  • Lovvorn JR, Watanuki Y, Kato A, Naito Y, Liggins GA (2004) Stroke patterns and regulation of swim speed and energy cost in free-ranging Brunnich’s guillemots. J Exp Biol 207:4679–4695

    Article  Google Scholar 

  • Luque SP (2007) Diving behaviour analysis in R. R News 7:8–14

    Google Scholar 

  • Luque SP, Fried R (2011) Recursive filtering for zero offset correction of diving depth time series with GNU R package diveMove. PLoS One 6:e15850

    Article  CAS  Google Scholar 

  • Menge BA, Daley BA, Wheeler PA, Dahlhoff E, Sanford E, Strub PT (1997) Benthic-pelagic links and rocky intertidal communities: bottom-up effects on top-down control? Proc Natl Acad Sci USA 94:14530–14535

    Article  CAS  Google Scholar 

  • Mori Y, Yoda K, Sato K (2001) Defining dive bouts using a sequential differences analysis. Behaviour 138:1451–1466

    Article  Google Scholar 

  • Mori Y, Takahashi A, Mehlum F, Watanuki Y (2002) An application of optimal diving models to diving behaviour of Brunnich’s guillemots. Anim Behav 64:739–745

    Article  Google Scholar 

  • Mori Y, Watanabe Y, Mitani Y, Sato K, Cameron MF, Naito Y (2005) A comparison of prey richness estimates for Weddell seals using diving profiles and image data. Mar Ecol Prog Ser 295:257–263

    Article  Google Scholar 

  • Navarro J, Votier SC, Aguzzi J, Chiesa JJ, Forero MG, Phillips RA (2013) Ecological segregation in space, time and trophic niche of sympatric planktivorous petrels. PLoS One 8(4):e62897

    Article  CAS  Google Scholar 

  • Pajaro M, Macchi GJ, Martos P (2005) Reproductive pattern of the Patagonian stock of Argentine hake (Merluccius hubbsi). Fish Res 72:97–108

    Article  Google Scholar 

  • Pennycuick CJ (1987) Flight of seabirds. In: Croxall JP (ed) Seabirds: feeding ecology and role in marine ecosystems. Cambridge University Press, Cambridge, pp 43–62

    Google Scholar 

  • Regular PM, Davoren GK, Hedd A, Montevecchi WA (2010) Crepuscular foraging by a pursuit-diving seabird: Tactics of common murres in response to the diel vertical migration of capelin. Mar Ecol Prog Ser 415:295–304

    Article  Google Scholar 

  • Regular PM, Hedd A, Montevecchi WA (2011) Fishing in the dark: a pursuit-diving seabird modifies foraging behaviour in response to nocturnal light levels. PLoS One 6:e26763

    Article  CAS  Google Scholar 

  • Ricklefs RE (1990) Seabirds life histories and the marine environment: some speculations. Colon Waterbirds 13:1–6

    Article  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

    Article  Google Scholar 

  • Sala JE, Wilson RP, Frere E, Quintana F (2012) Foraging effort in Magellanic penguins in coastal Patagonia, Argentina. Mar Ecol Prog Ser 464:273–287

    Article  Google Scholar 

  • Saunders T, Ydenberg R (1995) Consumption and caching of food in the northwestern crow (Corvus caurinus). Auk 112:778–779

    Google Scholar 

  • Schneider DC (1990) Seabirds and fronts: a brief overview. Polar Res 8(1):17–21

    Article  CAS  Google Scholar 

  • Schneider DC, Piatt JF (1986) Scale-dependent correlation of seabirds with schooling fish in a coastal ecosystem. Mar Ecol Prog Ser 32:237–246

    Article  Google Scholar 

  • Schoener TW (1971) Theory of feeding strategies. Annu Rev Ecol Evol Syst 2:369–404

    Google Scholar 

  • Thaxter CB, Wanless S, Daunt F, Harris MP, Benvenuti S, Watanuki Y, Gremillet D, Hamer KC (2010) Influence of wing loading on the trade-off between pursuit-diving and flight in common guillemots and razorbills. J Exp Biol 213:1018–1025

    Article  CAS  Google Scholar 

  • Waite TA, Ydenberg RC (1996) Foraging currencies and the load-size decision of scatter-hoarding grey jays. Anim Behav 51:903–916

    Article  Google Scholar 

  • Wanless S, Finney SK, Harris MP, McCafferty DJ (1999) Effect of the diel light cycle on the diving behaviour of two bottom feeding marine birds: the blue-eyed shag Phalacrocorax atriceps and the European shag P-aristotelis. Mar Ecol Prog Ser 188:219–224

    Article  Google Scholar 

  • Weimerskirch H (2002) The demography of seabirds and its relationship with the marine environment. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 115–135

    Google Scholar 

  • Weimerskirch H, Bonadonna F, Bailleul F, Mabille G, Dell’Omo G, Lipp HP (2002) GPS tracking of foraging albatrosses. Science 295:1259

    Article  CAS  Google Scholar 

  • Weimerskirch H, Bertrand S, Silva J, Carlos Marques J, Goya E (2010) Use of social information in seabirds: compass rafts indicate the heading of food patches. PLoS One 5:e9928

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wright PJ, Bailey MC (1991) Biology of sandeels in the vicinity of seabird colonies at Shetland

  • Ydenberg RC, Welham CVJ, Schmidhempel R, Schmidhempel P, Beauchamp G (1994) Time and energy constraints and the relationships between currencies in foraging theory. Behav Ecol 5:28–34

    Article  Google Scholar 

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Acknowledgments

We thank P. Collins who dedicated time for our projects during the 2012 field season. We also thank A. Flack, M. Mac, L. Yates, S. Harris, and C. Taylor for assistance in the field, the Wildlife Trust of South and West Wales, the Countryside Council for Wales and C. Taylor, Skomer Warden, for logistic support. T. Gaston, K. Elliott and E.E. van Loon provided comments on an earlier version of the paper. We also thank Paul Regular and two anonymous reviewers, whose comments improved the manuscript significantly. Financial support came from Japan Student Services Organization (AS), the American Animal Behavior Society (AS), the Department of Zoology and Merton College (AS), the Natural Sciences and Engineering Research Council of Canada (SAB), Environment Wales through the ‘Seabirds Cymru’ project which is co-ordinated by RSPB. All work was conducted after ethical approval by the Countryside Council for Wales, the Skomer Island Advisory Committee, and the British Trust for Ornithology’s Unconventional Methods Committee (BTO permits: Guilford, 5311; Perrins, 660; Shoji, 5939).

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Authors and Affiliations

  1. Animal Behaviour Research Group, Department of Zoology, University of Oxford, Oxford, Oxfordshire, OX1 3PS, UK

    Akiko Shoji, Ben Dean, Holly Kirk, Annette Fayet, Robin Freeman & Tim Guilford

  2. The Royal Society for the Protection of Birds, Etive House, Beechwood Park, Inverness, IV2 3BW, UK

    Ellie Owen

  3. The Royal Society for the Protection of Birds, The Lodge, Sandy, Bedfordshire, SG19 2DL, UK

    Mark Bolton

  4. Edward Grey Institute of Field Ornithology, Department of Zoology, University of Oxford, Oxford, Oxfordshire, OX1 3PS, UK

    Dave Boyle & Chris Perrins

  5. Institute of Zoology, Zoological Society of London, Regents Park, London, NW1 4RY, UK

    Robin Freeman

  6. Department of Mathematics and Statistics, University of Ottawa, Ottawa, ON, K1N 6N5, Canada

    Stéphane Aris-Brosou

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  1. Akiko Shoji
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  2. Ellie Owen
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  3. Mark Bolton
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  10. Stéphane Aris-Brosou
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Correspondence to Akiko Shoji or Tim Guilford.

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Communicated by S. Garthe.

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Shoji, A., Owen, E., Bolton, M. et al. Flexible foraging strategies in a diving seabird with high flight cost. Mar Biol 161, 2121–2129 (2014). https://doi.org/10.1007/s00227-014-2492-9

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