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Trophic ecology of Scopoli’s shearwaters during breeding in the Zembra Archipelago (northern Tunisia)

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Abstract

While breeding, seabirds are central-place foragers requiring resources to sustain high-energy requirements. Therefore, during this period, they are particularly sensitive to food-resource availability, which can vary within and between years. Intra- and inter-annual variations in Scopoli’s shearwater (Calonectris diomedea) trophic ecology were investigated at its largest colony (Zembra Island, 37°07′33″N, 10°48′23″E, Mediterranean Sea). Carbon and nitrogen isotope values were analysed in the blood (adults and chicks) and feathers (adult wing) during pre-laying, incubation, and chick-rearing in 2015 and 2016 to assess variations in stable isotope composition, isotopic niches, trophic levels, and diet inferred from isotope mixing models. Scopoli’s shearwaters showed variations in isotopes throughout the breeding season and among years, with incubation showing the highest δ13C and δ15N values, trophic levels, inter-annual isotopic niche consistency, and the most specific and narrowest isotopic niche. The difference in blood δ13C values between adults and chicks suggested trophic habitat segregation: adults feed inshore, while chicks are fed more oceanic prey. Stable-isotope mixing models based on three potential prey groups revealed that the diet could consist mainly of pelagic fish and crustaceans throughout the breeding season, whereas non-pelagic fish and cephalopods could be consumed more sporadically, mainly during incubation. Feather δ15N values suggested that the adult diets contained more zooplankton in 2014. These results demonstrated the Scopoli’s shearwater trophic ecology plasticity in response to the variable nutritional demands of breeding phases and changes in prey availability. Scopoli’s shearwaters may, thus, be valuable bio-indicators of small pelagic fish populations considered critically depleted in the Mediterranean.

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References

  • Abdennadher A, Ramírez F, Romdhane MS, Ruiz X, Jover L, Sanpera C (2010) Biomonitoring of coastal areas in Tunisia: stable isotope and trace element analysis in the Yellow-legged Gull. Mar Pollut Bull 60:440–447

    Article  CAS  PubMed  Google Scholar 

  • Afán I, Navarro J, Cardador L, Ramírez F, Kato A, Rodríguez B, Ropert-CoudertY Forero MG (2014) Foraging movements and habitat niche of two closely related seabirds breeding in sympatry. Mar Biol 161:657–668

    Article  Google Scholar 

  • Alonso H, Matias R, Granadeiro JP, Catry P (2009) Moult strategies of Cory’s Shearwaters Calonectris diomedea borealis: the influence of colony location, sex and individual breeding status. J Ornithol 150:329–337

    Article  Google Scholar 

  • 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 

  • APAL (2003) Etude des Plans de Gestion des Sites MEDWETCOAST—Site de Zembra. U.R.A.M. Press, Tunis, pp 1–61

    Google Scholar 

  • Arizaga J, Jover L, Aldalur A, Cuadrado JF, Herrero A, Sanpera C (2013) Trophic ecology of a resident Yellow-legged Gull (Larus michahellis) population in the Bay of Biscay. Mar Environ Res 87–88:19–25

    Article  CAS  PubMed  Google Scholar 

  • Báez JC, García-Barcelona S, Mendoza M, Ortiz de Urbina JM, Real R, Macías D (2014) Cory’s Shearwater by-catch in the Mediterranean Spanish commercial longline fishery: implications for management. Biodivers Conserv 23:661–681

    Article  Google Scholar 

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

    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 

  • 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 

  • Belda EJ, Sánchez A (2001) Seabird mortality on longline fisheries in the Western Mediterranean: factors affecting bycatch and proposed mitigating measures. Biol Conserv 98:357–363

    Article  Google Scholar 

  • Belgrano A, Scharler UM, Dunne J, Ulanowicz RE (2005) Aquatic food webs: an ecosystem approach. Oxford University Press, London

    Book  Google Scholar 

  • Bird CS, Veríssimo A, Magozzi S, Abrantes KG, Aguilar A, Al-Reasi H, Barnett DM, Bethea A, Biais G, Borrell A, Bouchoucha M, Boyle M, Brooks EJ, Brunnschweiler J, Bustamante P, Carlisle A, Catarino D, Caut S, Cherel Y, Chouvelon T, Churchill D, Ciancio J, Claes J, Colaço A, Courtney D, Cresson P, Daly R, De Necker L, Endo T, Figueiredo I, Frisch AJ, Hansen JH, Heithaus M, Hussey NE, Iitembu J, Juanes F, Kinney MJ, Kiszka JJ, Klarian SA, Kopp D, Leaf R, Li Y, Lorrain A, Madigan D, Maljković A, Malpica-Cruz L, Matich P, Meekan M, Menard F, Menezes GM, Munroe S, Newman M, Papastamatiou Y, Pethybridge H, Plumlee JD, Polo-Silva C, Quaeck-Davies K, Raoult V, Reum J, Torres-Rojas YE, Shiffman DS, Shipley ON, Speed CW, Staudinger M, Teffer A, Tilley A, Valls M, Vaudo JJ, Wai T-C, Wells RJD, Wyatt ASJ, Yool A, Trueman CN (2018) A global perspective on the trophic geography of sharks. Nat Ecol Evol 2:299–305

    Article  PubMed  Google Scholar 

  • Birdlife International (2016) Species factsheet: Calonectris diomedea. http://datazone.birdlife.org/species/factsheet/45061132. Accessed 15 Dec 2016

  • 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 

  • Borg J (1999) Philopatry in Cory’s Shearwater Calonectris diomedea in Malta. I1-Merill 29:11–15

    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 

  • Carboneras C, Derhé M, Ramírez I (2013) Update on the population status and distribution of Mediterranean shearwaters. Report to the Seventh Meeting of the ACAP Advisory Committee, La Rochelle

    Google Scholar 

  • Cardona L, Álvarez de Quevedo IA, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS One 7:e31329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Carravieri A, Bustamante P, Churlaud C, Cherel Y (2013) Penguins as bio-indicators of mercury contamination in the Southern Ocean: birds from the Kerguelen Islands as a case study. Sci Total Environ 454:141–148

    Article  CAS  PubMed  Google Scholar 

  • Cecere JG, Catoni C, Maggini I, Imperio S, Gaibani G (2013) Movement patterns and habitat use during incubation and chick-rearing of Cory’s Shearwaters from central Mediterranean: influence of seascape and breeding stage. J Zool 80:82–89

    Google Scholar 

  • Cecere JG, Gaibani G, Imperio S (2014) Effects of environmental variability and offspring growth on the movement ecology of breeding Scopoli’s Shearwater Calonectris diomedea. Curr Zool 60:622–630

    Article  Google Scholar 

  • Ceia FR, Paiva VH, Garthe S, Marques JC, Ramos JA (2014) Can variations in the spatial distribution at sea and isotopic niche width be associated with consistency in the isotopic niche of a pelagic seabird species? Mar Biol 161:1861–1872

    Article  Google Scholar 

  • Ceia FR, Paiva VH, Ceia RS, Hervías S, Garthe S, Marques JC, Ramos JA (2015) Spatial foraging segregation by close neighbours in a wide-ranging seabird. Oecologia 177:431–440

    Article  PubMed  Google Scholar 

  • Cherel Y, Hobson KA (2007) Geographical variation in stable carbon isotope composition 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 moulting 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, 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, Ramíre F (2014) Searching for the true diet of marine predators: incorporating Bayesian priors into stable isotope mixing models. PLoS One 9:e92665

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chouvelon T, Spitz J, Cherel Y, Caurant F, Sirmel R, Mèndez-Fernandez P, Bustamante P (2011) Inter-specific and ontogenic differences in δ13C and δ15N values and Hg and Cd concentrations in cephalopods. Mar Ecol Prog Ser 433:107–120

    Article  CAS  Google Scholar 

  • Coll M, Lotze HK, Romanuk TN (2008) Structural degradation in Mediterranean Sea food webs: testing ecological hypotheses using stochastic and mass-balance modelling. Ecosystems 11:939–960

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Costantini D, Dell’Omo G (2015) Oxidative stress predicts long-term resight probability and reproductive success in the Scopoli’s Shearwater (Calonectris diomedea). Conserv Physiol 3:cov024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Courbin N, Besnard A, Péron C, Saraux C, Fort J, Perret S, Tornos J, Grémillet D (2018) Short-term prey field lability constrains individual specialisation in resource selection and foraging site fidelity in a marine predator. Ecol Lett 21:1043–1054

    Article  PubMed  Google Scholar 

  • Cury PM, Boyd IL, Bonhommeau S, Anker-Nilssen T, Crawford RJM, Furness RW, Mills JA, Murphy EJ, Österblom H, Paleczny M, Piatt JF, Roux JP, Shannon L, Sydeman WJ (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706

    Article  CAS  PubMed  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 

  • Defos Du Rau P, Bourgeois K, Thévenet M, Ruffino L, Dromzée S, Ouni R, Abiadh A, Estéve R, Durand JP, Anselme L, Faggio G, Yahya JM, Rguibi H, Renda M, Miladi B, Hamrouni H, Alilech S, Nefla A, Jaouadi W, Agrebi S, Renou S (2015) Reassessment of the size of the Scopoli’s Shearwater population at its main breeding site resulted in a tenfold increase: implications for the species conservation. J Ornithol 156:877–892

    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 

  • Delord K, Pinet P, Pinaud D, Barbraud C, De Grissac S, LewdenA Cherel Y, Weimerskirch H (2016) Species-specific foraging strategies and segregation mechanisms of sympatric Antarctic Fulmarine petrels throughout the annual cycle. Ibis 158:569–586

    Article  Google Scholar 

  • Dimitrijević D, Paiva VH, Ramos JA, Seco J, Ceia FR, Chipev N, Valente T, Barbosa A, Xavier JC (2018) Isotopic niches of sympatric Gentoo and Chinstrap Penguins: evidence of competition for Antarctic krill? Polar Biol 41:1655–1669

    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  CAS  PubMed  PubMed Central  Google Scholar 

  • Fanelli E, Papiol V, Cartes JE, Rumolo P, López-Pérez C (2013) Trophic webs of deep-sea megafauna on mainland and insular slopes of the NW Mediterranean: a comparison by stable isotope analysis. Mar Ecol Prog Ser 490:199–221

    Article  CAS  Google Scholar 

  • Forero MG, Gonzalez-Solis 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 

  • Frederiksen M, Wanless S, Harris MP, Rothery P, Wilson NJ (2004) The role of industrial fisheries and environmental change in the decline of North Sea Black-legged Kittiwakes. J Appl Ecol 41:1129–1139

    Article  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

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

    Article  Google Scholar 

  • Gagné TO, Hyrenbach KD, Hagemann ME, Bass OL, Pimm SL, MacDonald M, Peck B, Van Houtan KS (2018) Seabird trophic position across three ocean regions tracks ecosystem differences. Front Mar Sci 5:317

    Article  Google Scholar 

  • GFCM (General Fisheries Commission for the Mediterranean) (2013) Report of the fifteenth session of the Scientific Advisory Committee. Rome, 8–11 April 2013. FAO Fisheries and Aquaculture Report No. 1042

  • Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West JB, Bowen GJ, Dawson TE, Tu KP (eds) Isoscapes: understanding movement, pattern and processes on Earth through isotope mapping. Springer, New York, pp 299–318

    Chapter  Google Scholar 

  • Granadeiro JP, Monteiro LR, Furness RW (1998) Diet and feeding ecology of Cory’s Shearwater Calonectris diomedea in the Azores, north-east Atlantic. Mar Ecol Prog Ser 166:267–276

    Article  Google Scholar 

  • Grémillet D, Péron C, Pons JB, Ouni R, Authier M, Thévenet M, Fort J (2014) Irreplaceable area extends marine conservation hotspot off Tunisia: insights from GPS-tracking Scopoli’s Shearwaters from the largest seabird colony in the Mediterranean. Mar Biol 161:2669–2680

    Article  Google Scholar 

  • Hairston NG Jr, Hairston NG Sr (1993) Cause–effect relationships in energy flow trophic structure and interspecific interactions. Am Nat 142:379–411

    Article  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, 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 diet using stable isotopes II: factors influencing diet-tissue fractionation. Condor 94:189–197

    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 

  • Hobson KA, Mclellan BN, Woods JG (2000) Using stable carbon (δ13C) and nitrogen (δ15N) isotopes to infer trophic relationships among Black and Grizzly bears in the upper Columbia River basin, British Columbia. Can J Zool 78:1332–1339

    Article  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 

  • Inger R, Bearhop S (2008) Applications of stable isotope analyses to avian ecology. Ibis 150:447–461

    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 

  • Karris G, Ketsilis-Rinis V, Kalogeropoulou A, Xirouchakis S, Machias A, Maina I, Kavadas S (2018) The use of demersal trawling discards as a food source for two scavenging seabird species: a case study of an eastern Mediterranean oligotrophic marine ecosystem. Avian Res 9:26

    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 

  • Laneri K, Louzao M, Martínez-Abraín A, Arcos JM, Belda EJ, Guallart J, Sánchez A, Giménez M, Maestre R, Oro D (2010) Trawling regime influences longline seabird by catch in the Mediterranean: new insights from a small-scale fishery. Mar Ecol Prog Ser 420:241–252

    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 164:211–228

    Article  Google Scholar 

  • Louzao M, Bécares J, Rodríguez B, Hyrenbach KD, Ruiz A, Arcos JM (2009) Combining vessel-based surveys and tracking data to identify key marine areas for seabirds. Mar Ecol Prog Ser 391:183–197

    Article  Google Scholar 

  • Louzao M, Arcos JM, Guijarro B, Valls M, Oro D (2011) Seabird-trawling interactions: factors affecting species-specific to regional community utilisation of fisheries waste. Fish Oceanogr 20:263–277

    Article  Google Scholar 

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

    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 

  • Mariano-Jelicich R, Favero M (2006) Assessing the diet of the Black Skimmer through different methodologies: is the analysis of pellets reliable? Waterbirds 29:81–87

    Article  Google Scholar 

  • Martínez-Abraín A, Maestre R, Oro D (2002) Demersal trawling waste as a food source for Western Mediterranean seabirds during the summer. ICES J Mar Sci 59:529–537

    Article  Google Scholar 

  • Mays G, Durand JM, Gomez G (2006) Première nidification du Puffin cendré (Calonectris diomedea) sur la façade atlantique française. Ornithos 13:316–319

    Google Scholar 

  • McMahon KW, Hamady LL, Thorrold SR (2013) Ocean ecogeochemistry: a review. Oceanogr Mar Biol Annu Rev 51:325–372

    Google Scholar 

  • Militão T, Bourgeois K, Roscales JL, González-Solís J (2012) Individual migratory patterns of two threatened seabirds revealed using stable isotope and geolocation analyses. Divers Distrib 19:317–329

    Article  Google Scholar 

  • Moore JC, De Ruiter PC (2012) Energetic food webs: an analysis of real and model ecosystems. Oxford University Press, Oxford

    Book  Google Scholar 

  • Mougin JL, Jouanin C (1997) Prospection alimentaire du puffin cendré Calonectris diomedea borealis de Selvagem Grande (30″ 09′ N, 15″ 52′ W) pendant l’incubation, par télémétrie satellitaire. C R Acad Sci Paris 320:825–831

    Article  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 (2009a) Seasonal changes in the diet of a critically endangered seabird and the importance of trawling discards. Mar Biol 156:2571–2578

    Article  Google Scholar 

  • Navarro J, Forero MG, González-Solís J, Igual JM, Bécares J, Hobson KA (2009b) Foraging segregation between two closely related shearwaters breeding in sympatry. Biol Lett 5:545–548

    Article  PubMed  PubMed Central  Google Scholar 

  • Navarro J, Coll M, Somes CJ, Olson RJ (2013) Trophic niche of squids: insights from isotopic data in marine systems worldwide. Deep Sea Res Part II 95:93–102

    Article  CAS  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 

  • 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 

  • Oro D, Ruiz X (1997) Exploitation of trawler discards by breeding seabirds in the north-western Mediterranean: differences between the Ebro Delta and the Balearic Islands areas. ICES J Mar Sci 54:695–707

    Article  Google Scholar 

  • Paiva VH, Geraldes P, Ramírez I, Merinho A, Garthe S, Ramos JA (2010a) Oceanographic characteristics of areas used by Cory’s Shearwater during short and long foraging trips in the North Atlantic. Mar Biol 157:1385–1399

    Article  Google Scholar 

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

    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  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 

  • Péron C, Grémillet D, Prudor A, Pettex E, Saraux C, Soriano-Redondo A, Authier M, Fort J (2013) Importance of coastal marine protected areas for the conservation of pelagic seabirds: the case of Vulnerable Yelkouan Shearwaters in the Mediterranean Sea. Biol Conserv 168:210–221

    Article  Google Scholar 

  • Pethybridge H, Choy CA, Logan JM, Allain V, Lorrain A, Bodin N, Somes CJ, Young J, Ménard F, Langlais C, Duffy L, Hobday AJ, Kuhnert P, Fry B, Menkes C, Olson RJ (2018) A global meta-analysis of marine predator nitrogen stable isotopes: relationships between trophic structure and environmental conditions. Glob Ecol Biogeogr 27:1043–1055

    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 (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Poupin N, Bos C, Mariotti F, Huneau JF, Tomé D, Fouillet H (2011) The nature of the dietary protein impacts the tissue-to-diet 15N discrimination factors in laboratory rats. PLoS One 6:e28046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quillfeldt P, Bugoni L, McGill RAR, 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 

  • Ramos R, González-Solís J, Ruiz X (2009a) Linking isotopic and migratory patterns in a pelagic seabird. Oecologia 160:97–105

    Article  PubMed  Google Scholar 

  • Ramos R, Militao T, González-Solís J, Ruiz X (2009b) Moulting strategies of a long-distance migratory seabird: the Mediterranean Cory’s Shearwater. Ibis 151:151–159

    Article  Google Scholar 

  • Ramos R, Ramírez F, Sanpera C, Jover L, Ruiz X (2009c) 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 R, Granadeiro JP, Nevoux M, Mougin JL, Dias MP, Catry P (2012) Combined spatio-temporal impacts of climate and longline fisheries on the survival of a trans-equatorial marine migrant. PLoS One 7:e40822

    Article  CAS  PubMed  PubMed Central  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 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 

  • Raya Rey A, Polito M, Archuby D, Coria N (2012) Stable isotopes identify age and sex specific dietary partitioning and foraging habitat segregation in Southern Giant Petrels breeding in Antarctica and Southern Patagonia. Mar Biol 159:1317–1326

    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 

  • 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 

  • Somes CJ, Schmittner A, Galbraith ED, Lehmann MF, Altabet MA, Montoya JP, Letelier RM, Mix AC, Bourbonnais A, Eby M (2010) Simulating the global distribution of nitrogen isotopes in the ocean. Glob Biogeochem Cycles 24:GB4019

    Article  CAS  Google Scholar 

  • Somes CJ, Schmittner A, Muglia J, Oschlies A (2017) A three-dimensional model of the marine nitrogen cycle during the last glacial maximum constrained by sedimentary isotopes. Front Mar Sci 4:108

    Article  Google Scholar 

  • Soriano-Redondo A, Cortés V, Reyes-González JM, Guallar S, Bécares J, Rodríguez B, Arcos JM, González-Solís J (2016) Relative abundance and distribution of fisheries influence risk of seabird bycatch. Sci Rep 6:37373

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2017) https://cran.r-project.org/doc/FAQ/R-FAQ.html#Citing-R. Accessed 17 Feb 2018

  • Thibault JC (1993) Natal philopatry in the Cory’s Shearwater (Calonectris diomedea diomedea) on Lavezzi Islands, Corsica. Colon Waterbird 16:77–82

    Article  Google Scholar 

  • Thompson DR, Phillips RA, Stewart FM, Waldron S (2000) Low δ13C composition 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 

  • Tiselius P, Fransson K (2015) Daily changes in δ15N and δ13C stable isotopes in copepods: equilibrium dynamics and variations of trophic level in the field. J Plankton Res 38:751–761

    Article  CAS  Google Scholar 

  • UNEP/MAP, SPA/RAC (2018) SPAMIs in the Mediterranean. http://www.rac-spa.org/spami. Accessed 28 Mar 2019

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182

    Article  PubMed  Google Scholar 

  • Wanless S, Harris M, Redman P, Speakman J (2005) Low energy values of fish as a probable cause of a major seabird breeding failure in the North Sea. Mar Ecol Prog Ser 294:1–8

    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 

  • 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 

  • Weiss F, Furness RW, Mcgill RA, Strange IJ, Masello JF, Quillfeldt P (2009) Trophic segregation of Falkland Islands seabirds: insights from stable isotope analysis. Polar Biol 32:1753–1763

    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 

  • Will AP, Kitaysky AS (2018) Variability in trophic level and habitat use in response to environmental forcing: isotopic niche dynamics of breeding seabirds in the southeastern Bering Sea. Mar Ecol Prog Ser 593:247–260

    Article  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 

  • Xavier JC, Magalhaes MC, Mendonça AS, Antunes M, Carvalho N, Machete M, Santos RS, Paiva VH, Hamer KC (2011) Changes in diet of Cory’s Shearwaters Calonectris diomedea breeding in the Azores. Mar Ornithol 39:129–134

    Google Scholar 

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Acknowledgements

The authors would like to acknowledge the financial support from the Fondation Total pour la Biodiversité through the TRIBAL project (“TRophic ecology and Impacts of Bycatch on the Avifauna communities of Zembra archipelago”). The authors also thank the staff of the Agence de Protection et d’Aménagement du Littoral (APAL) for providing authorisations for access to and sampling in the Zembra Archipelago marine protected area and for their help with logistical aspects, particularly Anis Zarrouk, Mahdi Bezi, and Hassan Zaghdoudi. Special thanks go to Habib Khiari, the fisherman who provided logistical assistance, to Ridha Ouni, and to Adel Ben Dhafer, the forest guardian of Zembra. We are grateful to Michelle Corson for improving the English and two anonymous reviewers for their constructive comments on the manuscript.

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Authors and Affiliations

  1. Faculté des Sciences de Tunis, Université Tunis El Manar, 2092, Tunis, Tunisia

    Intissar Thabet

  2. Institut National Agronomique de Tunisie, UR03AGRO1 Écosystèmes et Ressources Aquatiques, Université de Carthage, 1082, Tunis, Tunisia

    Intissar Thabet, Aida Abdennadher, Manel Gharsalli & Mohamed Salah Romdhane

  3. A dos d’Îles, Association for the Study and Conservation of Insular Biodiversity, Lançon-Provence, France

    Karen Bourgeois

  4. Institut de Recherche pour le Développement, UMR LEMAR (CNRS, UBO, IRD, Ifremer), IUEM, Plouzané, France

    François Le Loc’h & Jean-Marie Munaron

  5. Univ. Littoral Côte d’Opale, Univ. Lille, CNRS, UMR 8187, LOG, Laboratoire d’Océanologie et de Géosciences, 62930, Wimereux, France

    Frida Ben Rais Lasram

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  1. Intissar Thabet
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Thabet, I., Bourgeois, K., Le Loc’h, F. et al. Trophic ecology of Scopoli’s shearwaters during breeding in the Zembra Archipelago (northern Tunisia). Mar Biol 166, 61 (2019). https://doi.org/10.1007/s00227-019-3509-1

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