Skip to main content

Advertisement

SpringerLink
Log in

Flexible foraging strategies in a highly pelagic seabird revealed by seasonal isotopic niche variation

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Flexibility in foraging strategy is an important mechanism by which seabirds cope with spatiotemporal heterogeneity in food availability and the variable energetic constraints of their annual life cycle. Foraging strategy flexibility was investigated in the grey-faced petrel Pterodroma gouldi breeding on Ihumoana Island (36°53′S, 174°26′E) using stable isotope analyses. Intra- and inter-annual variations in stable isotope values, isotopic niches and diet inferred from isotope mixing models were studied by analysing δ15N and δ13C in adult wing feathers and blood, chick down and body feathers, and muscle from spontaneously regurgitated prey, collected during 2013 and 2014 breeding seasons. Grey-faced petrels exhibited variations in stable isotopes, isotopic niches and diet more markedly throughout their annual life cycle than between years. A trophic segregation occurred between adults and chicks presumably from adults feeding inshore and chicks being fed more oceanic prey of higher trophic level. Stable-isotope mixing models revealed that adult diet during the breeding season could consist mainly of ram’s horn squids Spirula spirula and chick diet of crustaceans, fish and other cephalopods being secondary prey throughout the breeding season. Adult male and female isotopic niches slightly differed. Finally, isotopic niche in adults during non-breeding was similar to that during breeding, suggesting non-breeding foraging areas located off the eastern Australian coast, around the limit between the Tasman and Coral seas. Our results demonstrated plasticity in the foraging strategy of grey-faced petrels in response to the changing nutritional demands of their annual cycle and to changes in oceanographic conditions likely driven by El Niño Southern Oscillation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Alonso H, Granadeiro JP, Paiva VH, Dias AS, Ramos JA, Catry P (2012) Parent-offspring dietary segregation of Cory’s shearwaters breeding in contrasting environments. Mar Biol 159:1197–1207

    Article  Google Scholar 

  • Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractionation of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458

    Article  CAS  PubMed  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, MacLeod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012

    Article  Google Scholar 

  • Bearhop S, Phillips RA, McGill R, Cherel Y, Dawson DA, Croxall JP (2006) Stable isotopes indicate sex-specific and long-term individual foraging specialisation in diving seabirds. Mar Ecol Prog Ser 311:157–164

    Article  Google Scholar 

  • Becker BH, Newman SH, Inglis S, Beissinger SR (2007) Diet-feather stable isotope (δ15N and δ13C) fractionation in common murres and other seabirds. Condor 109:451–456

    Article  Google Scholar 

  • Bond AL, Jones IL (2009) A practical introduction to stable-isotope analysis for seabird biologists: approaches, cautions and caveats. Mar Ornithol 37:183–188

    Google Scholar 

  • Bonnaud E, Bourgeois K, Vidal E, Kayser Y, Tranchant Y, Legrand J (2007) Feeding ecology of a feral cat population on a small Mediterranean island. J Mammal 88:1074–1081

    Article  Google Scholar 

  • Booth JM, Steinfurth A, Fusi M, Cuthbert RJ, McQuaid CD (2018) Foraging plasticity of breeding northern rockhopper penguins, Eudyptes moseleyi, in response to changing energy requirements. Polar Biol 41:1815–1826

    Article  Google Scholar 

  • Bourgeois K, Dromzée S, Welch JR, Russell JC (2017) Sex and geographic variation in grey-faced petrel (Pterodroma gouldi) morphometrics. Waterbirds 40:144–153

    Article  Google Scholar 

  • Bryant DM (1997) Energy expenditure in wild birds. Proc Nutr Soc 56:1025–1039

    Article  CAS  PubMed  Google Scholar 

  • Bugoni L, McGill RAR, Furness RW (2008) Effects of preservation methods on stable isotope signatures in bird tissues. Rapid Commun Mass Spectrom 22:2457–2462

    Article  CAS  PubMed  Google Scholar 

  • Carey MJ (2009) The effects of investigator disturbance on procellariiform seabirds: a review. N Z J Zool 36:367–377

    Article  Google Scholar 

  • Catard A, Weimerskirch H, Cherel Y (2000) Exploitation of distant Antarctic waters and close shelf-break waters by white-chinned petrels rearing chicks. Mar Ecol Prog Ser 194:249–261

    Article  Google Scholar 

  • Cerveira LR, Ramos JA, Rodrigues I, Almeida N, Araújo PM, dos Santos I, Vieira C, Pereira JM, Ceia FR, Geraldes P, Melo T, Paiva VH (2020) Inter-annual changes in oceanic conditions drives spatial and trophic consistency of a tropical marine predator. Mar Environ Res 162:105165

    Article  CAS  PubMed  Google Scholar 

  • Cherel Y, Hobson KA (2007) Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser 329:281–287

    Article  CAS  Google Scholar 

  • Cherel Y, Hobson KA, Bailleul F, Groscolas R (2005a) Nutrition, physiology, and stable isotopes: new information from fasting and molting penguins. Ecology 86:2881–2888

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Hassani S (2005b) Isotopic discrimination between food and blood and feathers of captive penguins: implications for dietary studies in the wild. Physiol Biochem Zool 78:106–115

    Article  PubMed  Google Scholar 

  • Cherel Y, Hobson KA, Weimerskirch H (2005c) Using stable isotopes to study resource acquisition and allocation in procellariiform seabirds. Oecologia 145:533–540

    Article  CAS  PubMed  Google Scholar 

  • Cherel Y, Le Corre M, Jaquemet S, Ménard F, Richard P, Weimerskirch H (2008) Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 366:281–291

    Article  CAS  Google Scholar 

  • Cherel Y, Connan M, Jaeger A, Richard P (2014a) Seabird year-round and historical feeding ecology: blood and feather δ13C and δ15N values document foraging plasticity of small sympatric petrels. Mar Ecol Prog Ser 505:267–280

    Article  Google Scholar 

  • Cherel Y, Jacquemet S, Maglio A, Jaeger A (2014b) Differences in δ13C and δ15N values between feathers and blood of seabird chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237

    Article  Google Scholar 

  • Chiaradia A, Forero MG, McInnes JC, Ramírez F (2014) Searching for the true diet of marine predators: incorporating Bayesian priors into stable isotope mixing models. PLoS ONE 9:e92665

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiaradia A, Ramírez F, Forero MG, Hobson KA (2016) Stable isotope (δ13C, δ15N) combined with conventional dietary approaches reveal plasticity in central-place foraging behavior of little penguins Eudyptula minor. Front Ecol Evol 3:154

    Article  Google Scholar 

  • Choy CA, Popp BN, Hannides CCS, Drazen JC (2015) Trophic structure and food resources of epipelagic and mesopelagic fishes in the North Pacific Subtropical Gyre ecosystem inferred from nitrogen isotopic compositions. Limnol Oceanogr 60:1156–1171

    Article  Google Scholar 

  • Congdon BC, Krockenberger AK, Smithers BV (2005) Dual-foraging and coordinated provisioning in a tropical Procellariiform, the wedge-tailed shearwater. Mar Ecol Prog Ser 301:293–301

    Article  Google Scholar 

  • Danckwerts DK, McQuaid CD, Connan M, Smale MJ, Le Corre M, Humeau L, Kaehler S, Juhasz CC, Orlowski S, Tourmetz J, Jaquemet S (2016) Intra-annual variation in the foraging ecology of the endangered endemic Barau’s petrel (Pterodroma baraui) from Réunion Island, south-western Indian Ocean: insights from a multifaceted approach. Mar Biol 163:18

    Article  Google Scholar 

  • Dehnhard N, Voigt CC, Poisbleau M, Demongin L, Quillfeldt P (2011) Stable isotopes in southern rockhopper penguins: foraging areas and sexual differences in the non-breeding period. Polar Biol 34:1763–1773

    Article  Google Scholar 

  • Dehnhard N, Ludynia K, Masello JF, Voigt CC, McGill RA, Quillfeldt P (2016) Plasticity in foraging behaviour and diet buffers effects of inter-annual environmental differences on chick growth and survival in Southern Rockhopper Penguins Eudyptes chrysocome chrysocome. Polar Biol 39:1627–1641

    Article  Google Scholar 

  • Doi H, Akamatsu F, González AL (2017) Starvation effects on nitrogen and carbon stable isotopes of animals: an insight from meta-analysis of fasting experiments. R Soc Open Sci 4:170633

    Article  PubMed  PubMed Central  Google Scholar 

  • Dunphy BJ, Taylor GA, Landers TJ, Sagar RL, Chilvers BL, Ranjard L, Rayner MJ (2015) Comparative seabird diving physiology: first measures of haematological parameters and oxygen stores in three New Zealand Procellariiformes. Mar Ecol Prog Ser 523:187–198

    Article  CAS  Google Scholar 

  • Forero MG, González-Solís J, Hobson KA, Doncazar JA, Bertellotti M, Blanco G, Bortolotti GR (2005) Stable isotopes reveal trophic segregation by sex and age in the southern giant petrel in two different food webs. Mar Ecol Prog Ser 296:107–113

    Article  Google Scholar 

  • France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: foodweb implications. Mar Ecol Prog Ser 124:307–312

    Article  Google Scholar 

  • Frederiksen M, Edwards M, Richardson AJ, Hallyday NC, Wanless S (2006) From plankton to top predators: bottom-up control of a marine food web across four trophic levels. J Anim Ecol 75:1259–1268

    Article  PubMed  Google Scholar 

  • Geary B, Leberg PL, Purcell KM, Walter ST, Karubian J (2020) Breeding brown pelicans improve foraging performance as energetic needs rise. Sci Rep 10:1686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • González-Medina E, Castillo-Guerrero JA, Herzka SZ, Fernández G (2017) Flexibility in food resource allocation in parents and selectivity for offspring: variations in δ15N and δ13C values during breeding of the blue-footed booby. Mar Biol 164:38

    Article  Google Scholar 

  • Graham B, Bury S (2019) Marine isoscapes for trophic and animal movement studies in the southwest Pacific Ocean. New Zealand Aquatic Environment and Biodiversity report no. 218. Fisheries New Zealand, Wellington

  • Grecian WJ, Taylor GA, Loh G, McGill RAR, Miskelly CM, Phillips RA, Thompson DR, Furness RW (2016) Contrasting migratory responses of two closely related seabirds to long-term climate change. Mar Ecol Prog Ser 559:231–242

    Article  CAS  Google Scholar 

  • Greene BS, Taylor GA, Earl R (2015) Distribution, population status and trends of grey faced petrel (Pterodroma macroptera gouldi) in northern North Island, New Zealand. Notornis 62:143–161

    Google Scholar 

  • Harper PC (1987) Feeding behaviour and other notes on 20 species of Procellariiformes at sea. Notornis 34:169–192

    Google Scholar 

  • Hedd A, Montevecchi WA, Phillips RA, Fifield DA (2014) Seasonal sexual segregation by monomorphic sooty shearwaters Puffinus griseus reflects different reproductive roles during the pre-laying period. PLoS ONE 9:e85572

    Article  PubMed  PubMed Central  Google Scholar 

  • Hertz E, Trudel M, Cox MK, Mazumder A (2015) Effects of fasting and nutritional restriction on the isotopic ratios of nitrogen and carbon: a meta-analysis. Ecol Evol 5:4829–4839

    Article  PubMed  PubMed Central  Google Scholar 

  • Hobson KA (1993) Trophic relationships among high Arctic seabirds: insights from tissue-dependent stable-isotope models. Mar Ecol Prog Ser 95:7–18

    Article  Google Scholar 

  • Hobson KA, Bond AL (2012) Extending an indicator: year-round information on seabird trophic ecology from multiple-tissue stable-isotope analyses. Mar Ecol Prog Ser 461:233–243

    Article  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes. I. Turnover of 13C in tissues. Condor 94:181–188

    Article  Google Scholar 

  • Hobson KA, Piatt JF, Pitocchelli J (1994) Using stable isotopes to determine seabird trophic relationships. J Anim Ecol 63:786–798

    Article  Google Scholar 

  • Hobson KA, Gibbs HL, Gloutney ML (1997) Preservation of blood and tissue samples for stable-carbon and stable nitrogen isotope analysis. Can J Zool 75:1720–1723

    Article  CAS  Google Scholar 

  • Hodum PJ, Hobson KA (2000) Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable isotope (δ15N and δ13C) analyses. Mar Ecol Prog Ser 198:273–281

    Article  Google Scholar 

  • Imber MJ (1973) The food of grey-faced petrels (Pterodroma macroptera gouldi (hutton)), with special reference to diurnal vertical migration of their prey. J Anim Ecol 42:645–662

    Article  Google Scholar 

  • Imber MJ (1976) Breeding biology of the grey-faced petrel Pterodroma macroptera gouldi. Ibis 118:51–64

    Article  Google Scholar 

  • Jackson AL, Inger R, Parnell AC, Bearhop S (2011) Comparing isotopic niche widths among and within communities: SIBER—Stable Isotope Bayesian Ellipses in R. J Anim Ecol 80:595–602

    Article  PubMed  Google Scholar 

  • Jaeger A, Blanchard P, Richard P, Cherel Y (2009) Using carbon and nitrogen isotopic values of body feathers to infer inter- and intra-individual variations of seabird feeding ecology during moult. Mar Biol 156:1233–1240

    Article  Google Scholar 

  • Jaeger A, Lecomte V, Weimerskirch H, Richard P, Cherel Y (2010) Seabird satellite tracking validates the use of latitudinal isoscapes to depict predators’ foraging areas in the Southern Ocean. Rapid Commun Mass Spectrom 24:3456–3460

    Article  CAS  PubMed  Google Scholar 

  • Jaeger A, Goutte A, Lecomte VJ, Richard P, Chastel O, Barbraud C, Weimerskirch H, Cherel Y (2014) Age, sex, and breeding status shape a complex foraging pattern in an extremely long-lived seabird. Ecology 95:2324–2333

    Article  PubMed  Google Scholar 

  • Jakubas D, Iliszko L, Wojczulanis-Jakubas K, Stempniewicz L (2012) Foraging by little auks in the distant marginal sea ice zone during the chick-rearing period. Polar Biol 35:73–81

    Article  Google Scholar 

  • Kaehler S, Pakhomov EA (2001) Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Mar Ecol Prog Ser 219:299–304

    Article  CAS  Google Scholar 

  • Kato A, Watanuki Y, Naito Y (2003) Annual and seasonal changes in foraging site and diving behavior in adélie penguins. Polar Biol 26:389–395

    Article  Google Scholar 

  • Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27

    Article  Google Scholar 

  • Kowalczyk ND, Chiaradia A, Preston TJ, Reina RD (2014) Linking dietary shifts and reproductive failure in seabirds: a stable isotope approach. Funct Ecol 28:755–765

    Article  Google Scholar 

  • Layman CA, Arrington DA, Montana CG, Post DM (2007) Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88:42–48

    Article  PubMed  Google Scholar 

  • Leal GR, Furness RW, McGill RAR, Santos RA, Bugoni L (2017) Feeding and foraging ecology of Trindade petrels Pterodroma arminjoniana during the breeding period in the South Atlantic Ocean. Mar Biol 164:211

    Article  Google Scholar 

  • MacArthur RH, Pianka ER (1966) On the optimal use of a patchy environment. Am Nat 100:603–610

    Article  Google Scholar 

  • Machovsky-Capuska GE, Miller MGR, Silva FRO, Amiot C, Stockin KA, Senior AM, Schuckard R, Melville D, Raubenheimer D (2018) The nutritional nexus: linking niche, habitat variability and prey composition in a generalist marine predator. J Anim Ecol 87:1286–1298

    Article  PubMed  Google Scholar 

  • MacLeod CJ, Adams J, Lyver P (2008) At-sea distribution of satellite-tracked grey-faced petrels, Pterodroma macroptera gouldi, captured on the Ruamaahua (Aldermen) islands, New Zealand. Pap Proc R Soc Tasman 142:73–88

    Google Scholar 

  • Magalhães MC, Santos RS, Hamer KC (2008) Dual-foraging of Cory’s shearwater in the Azores: feeding locations, behaviour at sea and implication for food provisioning of chicks. Mar Ecol Prog Ser 359:283–293

    Article  Google Scholar 

  • Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology, 2nd edn. Chapman and Hall, Boca Raton

    Google Scholar 

  • Marchant S, Higgins PJ (1990) Handbook of Australian, New Zealand and Antarctic birds, vol 1. Ratites to ducks. Part A, Ratites to petrels. Part B, Australian Pelican to ducks. Oxford University Press, Melbourne

    Google Scholar 

  • Miller MGR, Silva FRO, Machovsky-Capuska GE, Congdon BC (2018) Sexual segregation in tropical seabirds: drivers of sex-specific foraging in the Brown booby Sula leucogaster. J Ornithol 159:425–437

    Article  Google Scholar 

  • Monks JM, O’Donnell CFJ, Wright EF (2013) Selection of potential indicator species for measuring and reporting on trends in widespread native taxa in New Zealand. DOC research and development series 338. Department of Conservation, Wellington

    Google Scholar 

  • Navarro J, González-Solís J, Viscor G (2007) Nutritional and feeding ecology in Cory’s shearwater Calonectris diomedea during breeding. Mar Ecol Prog Ser 351:261–271

    Article  CAS  Google Scholar 

  • Navarro J, Louzao M, Igual JM, Oro D, Delgado A, Arcos JM, Genovart M, Hobson KA, Forero MG (2009) Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Mar Biol 156:2571–2578

    Article  Google Scholar 

  • Newsome SD, del Rio CM, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Eviron 5:429–436

    Article  Google Scholar 

  • Ohkouchi N, Tsuda R, Chikaraishi Y, Tanabe K (2013) A preliminary estimate of the trophic position of the deep-water ram’s horn squid Spirula spirula based on the nitrogen isotopic composition of amino acids. Mar Biol 160:773–779

    Article  CAS  Google Scholar 

  • Orians GH, Pearson NE (1979) On the theory of central place foraging. In: Horn DJ, Mitchell RD, Stairs GR (eds) Analysis of ecological systems. The Ohio State University Press, Columbus, pp 154–177

    Google Scholar 

  • Paiva VH, Xavier J, Geraldes P, Ramírez I, Garthe S, Ramos JA (2010) Foraging ecology of Cory’s shearwaters in different oceanic environments of the North Atlantic. Mar Ecol Prog Ser 410:257–268

    Article  Google Scholar 

  • Paiva VH, Ramos JA, Nava C, Neves V, Bried J, Magalhaes M (2018) Inter-sexual habitat and isotopic niche segregation of the endangered Monteiro’s storm-petrel during breeding. Zoology 126:29–35

    Article  CAS  PubMed  Google Scholar 

  • Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS ONE 5:e9672

    Article  PubMed  PubMed Central  Google Scholar 

  • Parnell AC, Phillips DL, Bearhop S, Semmens BX, Ward EJ, Moore JW, Jackson AL, Grey J, Kelly DJ, Inger R (2013) Bayesian stable isotope mixing models. Environmetrics 24:387–399

    Google Scholar 

  • Peery MZ, Newman SH, Storlazzi CD, Beissinger SR (2009) Meeting reproductive demands in a dynamic upwelling system: foraging strategies of a pursuit-diving seabird, the marbled murrelet. Condor 111:120–134

    Article  Google Scholar 

  • Phillips RA, McGill RAR, Dawson DA, Bearhop S (2011) Sexual segregation in distribution, diet and trophic level of seabirds: insights from stable isotope analysis. Mar Biol 158:2199–2208

    Article  Google Scholar 

  • Phillips RA, Lewis S, González-Solís J, Daunt F (2017) Causes and consequences of individual variability and specialization in foraging and migration strategies of seabirds. Mar Ecol Prog Ser 578:117–150

    Article  Google Scholar 

  • Pinet P, Jaquemet S, Phillips RA, Le Corre M (2012) Sex-specific foraging strategies throughout the breeding season in a tropical, sexually monomorphic small petrel. Anim Behav 83:979–989

    Article  Google Scholar 

  • Podlesak DW, McWilliams SR (2006) Metabolic routing of dietary nutrients in birds: effect of diet quality and macronutrient composition revealed using stable isotopes. Physiol Biochem Zool 79:534–549

    Article  CAS  PubMed  Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189

    Article  PubMed  Google Scholar 

  • Priddel D, Carlile N, Portelli D, Kim Y, O’Neill L, Bretagnolle V, Ballance LT, Phillips RA, Rayner MJ (2014) Pelagic distribution of Gould’s Petrel (Pterodroma leucoptera): linking sight records of seabirds with remote tracking data. Emu 114:360–370

    Article  Google Scholar 

  • Quillfeldt P (2002) Seasonal and annual variation in the diet of breeding and non-breeding Wilson’s storm-petrels on King George Island, South Shetland Islands. Polar Biol 25:216–221

    Article  Google Scholar 

  • Quillfeldt P, McGill RAR, Furness RW (2005) Diet and foraging areas of Southern Ocean seabirds and their prey inferred from stable isotopes: review and case study of Wilson’s storm-petrel. Mar Ecol Prog Ser 295:295–304

    Article  CAS  Google Scholar 

  • Quillfeldt P, Bugoni L, McGill RAR, Masello JF, Furness RW (2008a) Differences in stable isotopes in blood and feathers of seabirds are consistent across species, age and latitude: implications for food web studies. Mar Biol 155:593–598

    Article  CAS  Google Scholar 

  • Quillfeldt P, McGill RAR, Masello JF, Weiss F, Strange IJ, Brickle P, Furness RW (2008b) Stable isotope analysis reveals sexual and environmental variability and individual consistency in foraging of thin-billed prions. Mar Ecol Prog Ser 373:137–148

    Article  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009) Feeding ecology of yellow-legged gulls Larus michahellis in the western Mediterranean: a comparative assessment using conventional and isotopic methods. Mar Ecol Prog Ser 377:289–297

    Article  Google Scholar 

  • Ramos JA, Fagundes AI, Xavier JC, Fidalgo V, Ceia FR, Medeiros R, Paiva VH (2015) A switch in the Atlantic Oscillation correlates with inter-annual changes in foraging location and food habits of Macaronesian shearwaters (Puffinus baroli) nesting on two islands of the sub-tropical Atlantic Ocean. Deep Sea Res Part I 104:60–71

    Article  CAS  Google Scholar 

  • Ramos R, Carlile N, Madeiros J, Ramírez I, Paiva VH, Dinis H, Zino F, Biscoito M, Leal GR, Bugoni L, Jodice PGR, Ryan PG, González-Solís J (2017) It is the time for oceanic seabirds: tracking year-round distribution of gadfly petrels across the Atlantic Ocean. Divers Distrib 23:794–805

    Article  Google Scholar 

  • Ramos JA, Rodrigues I, Melo T, Geraldes P, Paiva VH (2018) Variation in ocean conditions affects chick growth, trophic ecology, and foraging range in Cape Verde Shearwater. Condor 120:283–290

    Article  Google Scholar 

  • Rayner MJ, Taylor GA, Gummer HD, Phillips RA, Sagar PM, Shaffer SA, Thompson DR (2012) The breeding cycle, year-round distribution and activity patterns of the endangered Chatham petrel (Pterodroma axillaris). Emu 112:107–116

    Article  Google Scholar 

  • Richoux NB, Jaquemet S, Bonnevie BT, Cherel Y, McQuaid CD (2010) Trophic ecology of grey-headed albatrosses from Marion Island, Southern Ocean: insights from stomach contents and diet tracers. Mar Biol 157:1755–1766

    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 

  • Roscales JL, Gómez-Diaz E, Neves V, González-Solíz J (2011) Trophic versus geographic structure in stable signatures of pelagic seabirds breeding in the northeast Atlantic. Mar Ecol Prog Ser 434:1–13

    Article  CAS  Google Scholar 

  • Ruiz-Cooley RI, Garcia KY, Hetherington ED (2011) Effects of lipid removal and preservatives on carbon and nitrogen stable isotope ratios of squid tissues: implications for ecological studies. J Exp Mar Biol Ecol 407:101–107

    Article  CAS  Google Scholar 

  • Russell JC, Welch JR, Dromzée S, Bourgeois K, Thoresen J, Earl R, Greene B, Westbrooke I, McNutt K (2017) Developing a national framework for monitoring the grey-faced petrel (Pterodroma gouldi) as an indicator species. DOC research and development series 350. Department of Conservation, Wellington

    Google Scholar 

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

    Article  Google Scholar 

  • Sears J, Hatch SA, O’brien DM, (2009) Disentangling effects of growth and nutritional status on seabird stable isotope ratios. Oecologia 159:41–48

    Article  PubMed  Google Scholar 

  • Shaffer SA, Costa DP, Weimerskirch H (2003) Foraging effort in relation to the constraints of reproduction in free-ranging albatrosses. Funct Ecol 17:66–74

    Article  Google Scholar 

  • Shoji A, Aris-Brosou S, Fayet A, Padget O, Perrins C, Guilford T (2015) Dual foraging and pair coordination during chick provisioning by Manx shearwaters: empirical evidence supported by a simple model. J Exp Biol 218:2116–2123

    PubMed  PubMed Central  Google Scholar 

  • Sibly RM, Witt CC, Wright NA, Venditti C, Jetz W, Brown JH (2012) Energetics, lifestyle, and reproduction in birds. Proc Natl Acad Sci USA 109:10937–10941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stearns SC (1992) The evolution of life histories. Oxford University Press, Oxford

    Google Scholar 

  • Steen H, Vogedes D, Broms F, Falk-Petersen S, Berge J (2007) Dovekies (Alle alle) breeding in a High Arctic fjord system: bimodal foraging strategies as a response to poor food quality? Polar Res 26:118–125

    Article  Google Scholar 

  • Thabet I, Bourgeois K, Le Loc’h F, Abdennadher A, Munaron J-M, Gharsalli M, Romdhane MS, Ben Rais Lasram F (2019) Trophic ecology of Scopoli’s shearwaters during breeding in the Zembra Archipelago (northern Tunisia). Mar Biol 166:61

    Article  Google Scholar 

  • Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low δ13C in pelagic seabirds: lipid ingestion as a potential source of 13C-depleted carbon in Procellariiformes. Mar Ecol Prog Ser 208:265–271

    Article  CAS  Google Scholar 

  • Tremblay Y, Cherel Y (2003) Geographic variation in the foraging behaviour, diet and chick growth of rockhopper penguins. Mar Ecol Prog Ser 251:279–297

    Article  Google Scholar 

  • Warham J (1977) The incidence, functions and ecological significance of petrel stomach oils. Proc N Z Ecol Soc 24:84–93

    Google Scholar 

  • Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, London

    Google Scholar 

  • Warham J (1996) The behaviour, population, biology and physiology of the petrels. Academic Press, London

    Google Scholar 

  • Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Cuenotchaillet F, Hindermeyer X, Judas J (1994) Alternate long and short foraging trips in pelagic seabird parents. Anim Behav 47:472–476

    Article  Google Scholar 

  • Whittow GC (2001) Seabird reproductive physiology and energetics. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton, pp 409–437

    Chapter  Google Scholar 

  • Williams CT, Buck CL, Sears J, Kitaysky AS (2007) Effects of nutritional restriction on nitrogen and carbon stable isotopes in growing seabirds. Oecologia 153:11–18

    Article  PubMed  Google Scholar 

  • Wood JR, Lawrence HA, Scofield RP, Taylor GA, Lyver POB, Gleeson DM (2017) Morphological, behavioural, and genetic evidence supports reinstatement of full species status for the Grey-faced Petrel, Pterodroma macroptera gouldi (Procellariiformes: Procellariidae). Zool J Linn Soc 179:201–216

    Google Scholar 

  • Yamamoto T, Hoshina K, Nishizawa B, Meathrel CE, Phillips RA, Watanuki Y (2015) Annual and seasonal movements of migrating short-tailed shearwaters reflect environmental variation in sub-Arctic and Arctic waters. Mar Biol 162:413–424

    Article  CAS  Google Scholar 

  • Zango L, Navarro-Herrero L, García-Vendrell M, Safi K, González-Solís J (2020) Niche partitioning and individual specialization among age, breeding status and sex classes in a long-lived seabird. Anim Behav 170:1–14

    Article  Google Scholar 

  • Zimmer I, Ropert-Coudert Y, Poulin N, Kato A, Chiaradia A (2011) 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

    Article  Google Scholar 

Download references

Acknowledgements

We are very grateful to the University of Auckland, the Royal Forest and Bird Protection Society of New Zealand and the European Union for funding this research. We are also very thankful to the Department of Conservation and island owners for granting permission and providing support to conduct this research. We thank all those who helped us during fieldwork, especially Marek Lang, Nalini Singh and Hendrik Schultz. We are grateful to the reviewers for their constructive comments on and improvements to the manuscript.

Funding

Funds and support were provided by the School of Biological Sciences, University of Auckland (SBS Internal Research Fund) and the Royal Forest and Bird Protection Society of New Zealand (JS Watson Trust). KB was supported by a Marie Curie Individual Fellowship (PIOF-GA-2012-328309).

Author information

Author notes

  1. Karen Bourgeois

    Present address: ECOMBI (Expertise Conservation des Oiseaux Marins et de la Biodiversité Insulaire), 62224, Equihen-Plage, France

  2. Jemma R. Welch

    Present address: Department of Conservation, Chatham Islands, 8942, New Zealand

  3. Sylvain Dromzée

    Present address: Parc Naturel des Estuaires Picards et de la Mer d’Opale, Office Français de la Biodiversité, 62360, Saint-Etienne-au-Mont, France

Authors and Affiliations

  1. School of Biological Sciences, University of Auckland, Auckland, 1142, New Zealand

    Karen Bourgeois, Jemma R. Welch, Sylvain Dromzée & James C. Russell

  2. Department of Conservation, Wellington, 6011, New Zealand

    Graeme A. Taylor

Authors
  1. Karen Bourgeois
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jemma R. Welch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvain Dromzée
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Graeme A. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. James C. Russell
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

KB and JCR conceived and designed the research. KB, JRW, SD and GAT carried out the fieldwork. KB and JRW analysed regurgitates. KB and JCR performed statistical analyses. KB wrote the manuscript and made the figures, with inputs from JCR and GAT. All authors contributed to and commented on manuscript drafts, and gave final approval for publication.

Corresponding author

Correspondence to Karen Bourgeois.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

Code availability

Not applicable.

Ethics approval

This work was conducted with ethics approval from the University of Auckland Animal Ethics Committee (AEC R898), and banding permit (#2010/021) and research permission (34780-RES and 38573-FAU) from the New Zealand Department of Conservation. Thus, all applicable international, national, and institutional guidelines for the sampling and the care of animals alive have been followed and all necessary approvals have been obtained.

Additional information

Responsible Editor: V. Paiva.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bourgeois, K., Welch, J.R., Dromzée, S. et al. Flexible foraging strategies in a highly pelagic seabird revealed by seasonal isotopic niche variation. Mar Biol 169, 28 (2022). https://doi.org/10.1007/s00227-021-04011-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-021-04011-w

Keywords

Search

Navigation