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Feeding and foraging ecology of Trindade petrels Pterodroma arminjoniana during the breeding period in the South Atlantic Ocean

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Abstract

Seabirds breeding in tropical environments experience high energetic demands, when foraging in an oligotrophic environment. The globally threatened Trindade petrel Pterodroma arminjoniana has its largest colony in Trindade Island (20°30′S–29°19′W) inside the oligotrophic South Atlantic Subtropical Gyre. Diet sampling methods, geolocator tracking and stable isotope analysis were used to describe its diet, compare foraging trips and distributions, and assess temporal variations in the trophic niche throughout the breeding period. Diet consisted mainly of squid and fish. The high species diversity and wide range of prey sizes consumed suggests the use of multiple foraging techniques. Stable isotope mixing models confirm that Trindade petrels rely mainly on squid throughout the breeding period. Its broad isotopic niche seems to reflect both a diverse diet and foraging range, since birds can reach up to 3335 km from the colony. Isotopic niche showed limited variation even in an 8-year interval, apparently due to oceanographic stability, although changes in the isotopic niche have demonstrated an adjustment to different conditions in different seasons. Petrels change foraging areas and prey during the breeding period: pre-incubating birds use more productive areas west of Trindade Island and obtain low trophic position prey; incubating petrels perform longer trips southward to consume prey of high trophic position; and chick-rearing petrels use areas around the island. These results demonstrate that to deal with high demand breeding in a colony surrounded by oligotrophic waters, Trindade petrels need to explore wide foraging areas and utilize a diverse diet, besides adjusting trophic niche according to breeding stage.

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References

  • Arruda WZ, Campos EJ, Zharkov V, Soutelino RG, Silveira IC (2013) Events of equatorward translation of the Vitoria Eddy. Cont Shelf Res 70:61–73

    Article  Google Scholar 

  • Ballance LT, Pitman RL, Fiedler PC (2006) Oceanographic influences on seabirds and cetaceans of the eastern tropical Pacific: a review. Prog Oceanogr 69:360–390

    Article  Google Scholar 

  • Barrett RT, Camphuysen KC, Anker-Nilssen T, Chardine JW, Furness RW, Garthe S, Veit RR (2007) Diet studies of seabirds: a review and recommendations. ICES J Mar Sci 64:1675–1691

    Article  Google Scholar 

  • Barth R (1958) Observações biológicas e meteorológicas feitas na Ilha de Trindade. Mem Inst Oswaldo Cruz 56:261–279

    Article  Google Scholar 

  • Bearhop S, Teece MA, Waldron S, Furness RW (2000) Influence of lipid and uric acid on δ 13C and δ 15N values of avian blood: implications for trophic studies. Auk 117:504–507

    Google Scholar 

  • Bester AJ, Priddel D, Klomp NI (2010) Diet and foraging behaviour of the Providence petrel Pterodroma solandri. Mar Ornithol 39:163–172

    Google Scholar 

  • Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023

    Article  Google Scholar 

  • Bouali M, Sato OT, Polito PS (2017) Temporal trends in sea surface temperature gradients in the South Atlantic Ocean. Remote Sens Environ 194:100–114

    Article  Google Scholar 

  • Bourgeois K, Vorenger J, Faulquier L, Legrand J, Vidal E (2011) Diet and contamination of the Yelkouan shearwater Puffinus yelkouan in the Hyères archipelago, Mediterranean Basin, France. J Ornithol 152:947–953

    Article  Google Scholar 

  • British Antarctic Survey (2008) M-Series BASTrack software

  • Brown RM, Nichols RA, Faulkes CG, Jones CG, Bugoni L, Tatayah V, Gottelli D, Jordan WC (2010) Range expansion and hybridization in Round Island petrels (Pterodroma spp.): evidence from microsatellite genotypes. Mol Ecol 19:3157–3170

    Article  Google Scholar 

  • Brown SC, Bizzarro JJ, Cailliet GM, Ebert DA (2012) Breaking with tradition: redefining measures for diet description with a case study of the Aleutian skate Bathyraja aleutica (Gilbert 1896). Environ Biol Fish 95:3–20

    Article  Google Scholar 

  • Brunetti NE, Ivanovic ML, Aubone A, Pascual LN (2006) Reproductive biology of red squid (Ommastrephes bartramii) in the southwest Atlantic. Rev Invest Desarr Pesq 18:5–19

    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  Google Scholar 

  • Bugoni L, McGill RAR, Furness RW (2010) The importance of pelagic longline fishery discards for a seabird community determined through stable isotope analysis. J Exp Mar Biol Ecol 391:190–200

    Article  Google Scholar 

  • Bugoni L, Griffiths K, Furness RW (2011) Sex-biased incidental mortality of albatrosses and petrels in fisheries: differential distributions at sea or differential access to baits mediated by sexual size dimorphism? J Ornithol 152:261–268

    Article  Google Scholar 

  • Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519

    Article  Google Scholar 

  • Castro JWA (2009) Geologia ambiental das ilhas oceânicas de Trindade e Fernando de Noronha, Brasil. In: Mohr LV, Castro JWA, Costa PMS, Alves RJV (eds) Ilhas oceânicas brasileiras: da pesquisa ao manejo. Ministério do Meio Ambiente, Brasília

    Google Scholar 

  • Catry T, Ramos JA, Jaquemet S, Faulquier L, Berlincourt M, Hauselmann A, Pinet P, Le Corre M (2009) Comparative foraging ecology of a tropical seabird community of the Seychelles, western Indian Ocean. Mar Ecol Prog Ser 374:259–272

    Article  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, Bocher P, Trouvé C, Weimerskirch H (2002) Diet and feeding ecology of blue petrels Halobaena caerulea at Iles Kerguelen, southern Indian Ocean. Mar Ecol Prog Ser 228:283–299

    Article  Google Scholar 

  • Cherel Y, Hobson KA, Hassani S (2005) 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  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

    Article  Google Scholar 

  • Cherel Y, Le Corre M, Jaquemet S, Menard 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, Xavier JC, De Grissac S, Trouvé C, Weimerskirch H (2017) Feeding ecology, isotopic niche, and ingestion of fishery-related items of the wandering albatross Diomedea exulans at Kerguelen and Crozet Islands. Mar Ecol Prog Ser 565:197–215

    Article  Google Scholar 

  • Clarke MR (1966) A review of the systematics and ecology of oceanic squids. Adv Mar Biol 4:91–300

    Article  Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopod beaks. Clarendon Press, Oxford

    Google Scholar 

  • Clarke MR, Denton EJ, Gilpin-Brown JB (1979) On the use of ammonium for buoyancy in squids. J Mar Biol Assoc UK 59:259–276

    Article  CAS  Google Scholar 

  • Coelho M (1985) Review of the influence of oceanographic factors on cephalopod distribution and life cycles. Northw Atl Fish Org 897:1–16

    Google Scholar 

  • Colabuono FI, Vooren CM (2007) Diet of black-browed Thalassarche melanophrys and Atlantic yellow-nosed T. chlororhynchos albatrosses and white-chinned Procellaria aequinoctialis and spectacled P. conspicillata petrels off southern Brazil. Mar Ornithol 35:9–20

    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 

  • Croxall JP, Butchart SH, Lascelles B, Stattersfield AJ, Sullivan B, Symes A, Taylor P (2012) Seabird conservation status, threats and priority actions: a global assessment. Bird Conserv Int 22:1–34

    Article  Google Scholar 

  • Danckwerts DK, McQuaid CD, Connan M, Smale MJ, Le Corre M, Humeau L, 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 

  • Eder EB, Lewis MN (2005) Proximate composition and energetic value of demersal and pelagic prey species from the SW Atlantic Ocean. Mar Ecol Prog Ser 291:43–52

    Article  CAS  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 

  • Flood B, Fisher A (2013) Multimedia identification guide to North Atlantic seabirds: Pterodroma petrels. Scilly Pelagics, Isles of Scilly

    Google Scholar 

  • Fonseca-Neto FP (2004) Aves marinhas da ilha Trindade. In: Branco JO (ed) Aves marinhas e insulares brasileiras: bioecologia e conservação. UNIVALI Editora, Itajaí

    Google Scholar 

  • Forero MG, González-Solís J, Hobson KA, Donázar 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 

  • Franks PJ (1992) Sink or swim: accumulation of biomass at fronts. Mar Ecol Prog Ser 82:1–12

    Article  Google Scholar 

  • Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121

    Article  Google Scholar 

  • Furness RW (2007) Responses of seabirds to depletion of food fish stocks. J Ornithol 148:247–252

    Article  Google Scholar 

  • Gaston AJ, Elliott KH (2014) Seabird diet changes in northern Hudson Bay, 1981–2013, reflect the availability of schooling prey. Mar Ecol Prog Ser 513:211–223

    Article  Google Scholar 

  • Gill F, Donsker D (2017) IOC World Bird List. Available at http://www.worldbirdnames.org

  • González-Solís J, Croxall JP, Wood AG (2000) Foraging partitioning between giant petrels Macronectes spp. and its relationship with breeding population changes at Bird Island, South Georgia. Mar Ecol Prog Ser 204:279–288

    Article  Google Scholar 

  • Greenaway P (1985) Calcium balance and moulting in the Crustacea. Biol Rev 60:425–454

    Article  CAS  Google Scholar 

  • Hennicke JC, Weimerskirch H (2014) Coping with variable and oligotrophic tropical waters: foraging behaviour and flexibility of the Abbott’s booby Papasula abbotti. Mar Ecol Prog Ser 499:259–273

    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 

  • 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) Comparison of prey of the black Procellaria petrels of New Zealand. New Zeal J Mar Freshw Res 10:119–130

    Article  Google Scholar 

  • Imber MJ, Jolly JN, Brooke MDL (1995) Food of three sympatric gadfly petrels (Pterodroma spp.) breeding on the Pitcairn Islands. Biol J Linn Soc 56:233–240

    Article  Google Scholar 

  • IUCN (2016) The IUCN Red List of Threatened Species. Version 2016–3

  • 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  Google Scholar 

  • Jaquemet S, Le Corre M, Weimerskirch H (2004) Seabird community structure in a coastal tropical environment: importance of natural factors and fish aggregating devices (FADs). Mar Ecol Prog Ser 268:281–292

    Article  Google Scholar 

  • Jaquemet S, Potier M, Cherel Y, Kojadinovic J, Bustamante P, Richard P, Catry T, Ramos JA, Le Corre M (2008) Comparative foraging ecology and ecological niche of a superabundant tropical seabird: the sooty tern Sterna fuscata in the southwest Indian Ocean. Mar Biol 155:505–520

    Article  Google Scholar 

  • Jereb P, Roper CFE (2010) Cephalopods of the world. An annotated and illustrated catalogue of species known to date. Myopsid and Oegopsid squids. FAO species catalogue for fishery purposes

  • Jodice PG, Ronconi RA, Rupp E, Wallace GE, Satgé Y (2015) First satellite tracks of the endangered black-capped petrel. Endang Species Res 29:23–33

    Article  Google Scholar 

  • Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108

    Article  Google Scholar 

  • Klages NTW, Cooper J (1997) Diet of the Atlantic petrel Pterodroma incerta during breeding at South Atlantic Gough Island. Mar Ornithol 25:13–16

    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 

  • Krüger L, Paiva VH, Colabuono FI, Petry MV, Montone RC, Ramos JA (2016) Year-round spatial movements and trophic ecology of Trindade petrels (Pterodroma arminjoniana). J Field Ornithol 87:404–416

    Article  Google Scholar 

  • Lalli C, Parsons TR (1997) Biological oceanography: an introduction. Butterworth-Heinemann, Oxford

    Google Scholar 

  • Lascelles BG, Taylor PR, Miller MGR, Dias MP, Oppel S, Torres L, Hedd A, Le Corre M, Phillips RA, Shaffer SA, Weimerskirch H, Small C (2016) Applying global criteria to tracking data to define important areas for marine conservation. Divers Distrib 22:422–431

    Article  Google Scholar 

  • Lavrado HP, Viana MS (2007) Atlas de invertebrados marinhos da região central da Zona Econômica Exclusiva brasileira. Museu Nacional, Rio de Janeiro

    Google Scholar 

  • Le Corre M, Cherel Y, Lagarde F, Lormée H, Jouventin P (2003) Seasonal and inter-annual variation in the feeding ecology of a tropical oceanic seabird, the red-tailed tropicbird Phaethon rubricauda. Mar Ecol Prog Ser 255:289–301

    Article  Google Scholar 

  • Leal JH, Bouchet P (1991) Distribution patterns and dispersal of prosobranch gastropods along a seamount chain in the Atlantic Ocean. J Mar Biol Assoc UK 71:11–25

    Article  Google Scholar 

  • Lewis S, Benvenuti S, Dall-Antonia L, Griffiths R, Money L, Sherratt TN, Wanless S, Hamer KC (2002) Sex-specific foraging behaviour in a monomorphic seabird. Proc R Soc Lond B Biol Sci 269:1687–1693

    Article  CAS  Google Scholar 

  • Lipinski MR, Jackson S (1989) Surface-feeding on cephalopods by procellariiform seabirds in the southern Benguela region, South Africa. J Zool (Lond) 218:549–563

    Article  Google Scholar 

  • Lu CC, Ickeringill R (2002) Cephalopod beak identification and biomass estimation techniques: tools for dietary studies of southern Australian finfishes. Mus Vic Sci Rep 6:1–65

    Google Scholar 

  • Luigi G, Bugoni L, Fonseca-Neto FP, Teixeira DM (2009) Biologia e conservação do petrel-de-trindade, Pterodroma arminjoniana, na ilha da Trindade, Atlântico sul. In: Mohr LV, Castro JWA, Costa PMS, Alves RJV (eds) Ilhas oceânicas brasileiras: da pesquisa ao manejo, vol 2. Ministério do Meio Ambiente, Brasília

    Google Scholar 

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

    Article  Google Scholar 

  • Mallory ML, Forbes MR, Ankney CD, Alisauskas RT (2008) Nutrient dynamics and constraints on the pre-laying exodus of high Arctic northern fulmars. Aquat Biol 4:211–223

    Article  Google Scholar 

  • Mancini PL, Hobson KA, Bugoni L (2014) Role of body size in shaping the trophic structure of tropical seabird communities. Mar Ecol Prog Ser 497:243–257

    Article  Google Scholar 

  • Mancini PL, Serafini PP, Bugoni L (2016) Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Rev Bras Ornitol 24:94–115

    Google Scholar 

  • Matsuura Y, Nakatani K, Tamassia STJ (1980) Distribuição sazonal de zooplâncton, ovos e larvas de peixes na região centro-sul do Brasil (1975–77). Bolm Inst Oceanogr 29:231–235

    Article  Google Scholar 

  • MMA (Ministério do Meio Ambiente) (2014) Lista Nacional Oficial de Espécies da Fauna Ameaçadas de Extinção, Brasília

  • 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 

  • Negrete P, Sallaberry M, Barceló G, Maldonado K, Perona F, McGill RAR, Quillfeldt P, Sabat P (2017) Temporal variation in isotopic composition of Pygoscelis penguins at Ardley Island, Antarctic: are foraging habits impacted by environmental change? Polar Biol 40:903–916

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Nogueira MM, Souza CSD, Mafalda-Jr PO (2012) The influence of abiotic and biotic factors on the composition of Tetraodontiformes larvae (Teleostei) along the Brazilian northeast Exclusive Economic Zone (1°N–14°S). Panam J Aquat Sci 7:10–20

    Google Scholar 

  • Nonaka RH, Matsuura Y, Suzuki K (2000) Seasonal variation in larval fish assemblages in relation to oceanographic conditions in the Abrolhos Bank region off eastern Brazil. Fish Bull 98:767–767

    Google Scholar 

  • Ojowski U, Eidtmann C, Furness R, Garthe S (2001) Diet and nest attendance of incubating and chick-rearing northern fulmars (Fulmarus glacialis) in Shetland. Mar Biol 139:1193–1200

    Article  Google Scholar 

  • Olson DB, Backus RH (1985) The concentrating of organisms at fronts: a cold-water fish and a warm-core Gulf Stream ring. J Mar Res 43:113–137

    Article  Google Scholar 

  • Opitz S (1996) Trophic interactions in Caribbean coral reefs. ICLARM Tech, Philippines

    Google Scholar 

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

    Google Scholar 

  • Paiva VH, Xavier J, Geraldes P, Ramirez 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, Geraldes P, Rodrigues I, Melo T, Melo J, Ramos JA (2015) The foraging ecology of the endangered Cape Verde shearwater, a sentinel species for marine conservation off West Africa. PLoS ONE 10:e0139390

    Article  CAS  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  CAS  Google Scholar 

  • Peterson RG, Stramma L (1991) Upper-level circulation in the South Atlantic Ocean. Prog Oceanogr 26:1–73

    Article  Google Scholar 

  • Phillips RA, Xavier JC, Croxall JP (2003) Effects of satellite transmitters on albatrosses and petrels. Auk 120:1082–1090

    Article  Google Scholar 

  • Phillips RA, Silk JRD, Croxall JP, Afanasyev V, Briggs DR (2004) Accuracy of geolocation estimates for flying seabirds. Mar Ecol Prog Ser 266:265–272

    Article  Google Scholar 

  • Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527

    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 

  • Pierce GJ, Valavanis VD, Guerra A, Jereb P, Orsi-Relini L, Bellido JM, Katara I, Piatkowski U, Pereira J, Balguerias E, Sobrino I, Lefkaditou E, Wang J, Santurtun M, Boyle PR, Hastie LC, MacLeod CD, Smith JM, Viana M, González AF, Zuur AF (2008) A review of cephalopod–environment interactions in European seas. Hydrobiologia 612:49–70

    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 

  • Quillfeldt P, Bugoni L, McGill RA, Masello JF, Furness RW (2008) 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 

  • Ramírez I, Paiva VH, Menezes D, Silva I, Phillips RA, Ramos JA, Garthe S (2013) Year-round distribution and habitat preferences of the Bugio petrel. Mar Ecol Prog Ser 476:269–284

    Article  Google Scholar 

  • Ramírez I, Paiva VH, Fagundes I, Menezes D, Silva I, Ceia FR, Phillips RA, Ramos JA, Garthe S (2016) Conservation implications of consistent foraging and trophic ecology in a rare petrel species. Anim Conserv 19:139–152

    Article  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 

  • Rayner MJ, Hauber ME, Clout MN, Seldon DS, van Dijken S, Bury S, Phillips RA (2008) Foraging ecology of the Cook’s petrel Pterodroma cookii during the austral breeding season: a comparison of its two populations. Mar Ecol Prog Ser 370:271–284

    Article  Google Scholar 

  • Rayner MJ, Hartill BW, Hauber ME, Phillips RA (2010) Central place foraging by breeding Cook’s petrel Pterodroma cookii: foraging duration reflects range, diet and chick meal mass. Mar Biol 157:2187–2194

    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 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Robertson GS, Bolton M, Grecian WJ, Monaghan P (2014) Inter-and intra-year variation in foraging areas of breeding kittiwakes (Rissa tridactyla). Mar Biol 161:1973–1986

    Article  CAS  Google Scholar 

  • Roper CF (1963) Observations on bioluminescence in Ommastrephes pteropus (Steenstrup, 1855), with notes on its occurrence in the family Ommastrephidae (Mollusca: Cephalopoda). Bull Mar Sci 13:343–353

    Google Scholar 

  • Santos RA (1999) Cefalópodes nas relações tróficas do sul do Brasil. Fundação Universidade do Rio Grande - FURG, PhD Thesis, Rio Grande

  • Santos RA, Haimovici M (2001) Cephalopods in the diet of marine mammals stranded or incidentally caught along southeastern and southern Brazil. Fish Res 52:99–112

    Article  Google Scholar 

  • Santos RA, Haimovici M (2002) Cephalopods in the trophic relations off southern Brazil. Bull Mar Sci 71:753–770

    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  Google Scholar 

  • Shealer DA (2001) Foraging behavior and food of seabirds. In: Schreiber EA, Burger J (eds) Biology of marine birds. CRC Press, Boca Raton

    Google Scholar 

  • Silva JBP (2011) Stomatopoda (Crustacea-Hoplocarida) no nordeste brasileiro: morfometria como ferramenta taxonômica. Universidade Federal da Paraíba, MSc. Dissertation, João Pessoa

  • Silveira ICAD, Schmidt ACK, Campos EJD, Godoi SSD, Ikeda Y (2000) A Corrente do Brasil ao largo da costa leste brasileira. Braz J Oceanogr 48:171–183

    Article  Google Scholar 

  • Sorensen MC, Hipfner JM, Kyser TK, Norris DR (2009) Carry-over effects in a Pacific seabird: stable isotope evidence that pre-breeding diet quality influences reproductive success. J Anim Ecol 78:460–467

    Article  Google Scholar 

  • Soutelino RG, Silveira ICA, Gangopadhyay A, Miranda JA (2011) Is the Brazil Current eddy-dominated to the north of 20°S? Geophys Res Lett 38:L03607

    Article  Google Scholar 

  • Strass VH (1992) Chlorophyll patchiness caused by mesoscale upwelling at fronts. Deep Sea Res A Oceanogr Res 39:75–96

    Article  Google Scholar 

  • Thiebot JB, Weimerskirch H (2013) Contrasted associations between seabirds and marine mammals across four biomes of the southern Indian Ocean. J Ornithol 154:441–453

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ 15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  Google Scholar 

  • Voss NA, Vecchione M, Toll RB, Sweeney MJ (1998) Systematics and biogeography of cephalopods. Smithsonian Contributions to Zoology. Smithsonian Institution Press, Washington

    Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Weimerskirch H, Jouventin P, Stahl JC (1986) Comparative ecology of the six albatross species breeding on the Crozet Islands. Ibis 128:195–213

    Article  Google Scholar 

  • Weimerskirch H, Chastel O, Ackermann L, Chaurand T, Cuenot-Chaillet 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

    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  Google Scholar 

  • Xavier JC, Wood AG, Rodhouse PG, Croxall JP (2007) Interannual variations in cephalopod consumption by albatrosses at South Georgia: implications for future commercial exploitation of cephalopods. Mar Freshw Res 58:1136–1143

    Article  Google Scholar 

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Acknowledgements

We are grateful to Hudson T. Pinheiro for fish identification, Dr. Geoff Hancock for insect identification and Dr. Paul Kinas for help with statistics; Brazilian Navy and Comissão Interministerial para os Recursos do Mar (CIRM/SECIRM) by logistic support during sampling expeditions. We also thank Eduardo R. Secchi, Manuel Haimovici and Luciano Dalla Rosa for the revision and comments on the manuscript. This research is part of the PhD thesis written by G.R.L. under the guidance of L.B. and was authorized under the license number 22697-5 (SISBIO—Sistema de Autorização e Informação em Biodiversidade).

Funding

This project had been funded by Natural Environment Research Council (NERC-UK, Grant Number EK81-07/05) and the Brazilian National Research Council (CNPq, Grants 557152/2009-7 and 405555/2012-1). G.R. Leal received financial support from the Coordenação de Aperfeiçoamento de Pessoal de Nível SuperiorCAPES (Ministry of Education). L. Bugoni received a Research Fellowship from CNPq (PQ 310550/2015-7).

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Leal, G.R., Furness, R.W., McGill, R.A.R. et al. Feeding and foraging ecology of Trindade petrels Pterodroma arminjoniana during the breeding period in the South Atlantic Ocean. Mar Biol 164, 211 (2017). https://doi.org/10.1007/s00227-017-3240-8

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