Marine Biology

, Volume 161, Issue 11, pp 2669–2680 | Cite as

Irreplaceable area extends marine conservation hotspot off Tunisia: insights from GPS-tracking Scopoli’s shearwaters from the largest seabird colony in the Mediterranean

  • David GrémilletEmail author
  • Clara Péron
  • Jean-Baptiste Pons
  • Ridha Ouni
  • Matthieu Authier
  • Mathieu Thévenet
  • Jérôme Fort
Original Paper


Recent meta-analyses identified conservation hotpots at the scale of the Mediterranean, yet those may be crude by lack of detailed information about the spatial ecology of the species involved. Here, we identify an irreplaceable marine area for >95 % of the world population of the Scopoli’s shearwater (Calonectris diomedea), which is endemic to the Mediterranean and breeds on the island of Zembra off Tunis. To this end, we studied the three-dimensional at-sea movements of 50 breeding adults (over a total of 94 foraging trips) in 2012 and 2013, using GPS and temperature–depth recorders. Feathers were also collected on all birds to investigate their trophic status. Despite Zembra being the largest seabird colony in the Mediterranean (141,000 pairs), the per capita home-range of Scopoli’s shearwaters foraging from this colony was not larger than that of birds from much smaller colonies, indicating highly beneficial feeding grounds in the Gulf of Tunis and off Cap Bon. Considering depleted Mediterranean small pelagic fish stocks, supposed to be Scopoli’s shearwater prey base, we therefore speculate that birds may now also largely feed on zooplankton, something which is supported by our stable isotopic analyses. Crucially, shearwater at-sea feeding and resting areas showed very little overlap with a conservation hotspot recently defined on the western side of the Gulf of Tunis using meta-analyses of species distributions relative to anthropogenic threats. We therefore propose a major extension to this conservation hotspot. Our study stresses the importance of detailed biotelemetry studies of marine megafauna movement ecology for refining large-scale conservation schemes such as marine protected area networks.


Isotopic Niche Small Pelagic Fish Important Bird Area Yelkouan Shearwater Isotopic Niche Width 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



Fieldwork for this study was funded by the PIM initiative (Petites Iles de Méditerranée), while all electronic equipment was provided by the CEFE-CNRS Montpellier. Clara Péron was funded by the French agency for marine protected areas (AAMP) within the “Programme PACOMM, Natura 2000 en mer”. We are grateful to Ana Rodrigues for ‘irreplaceable’ advice, Marta Coll for providing us with the exact outline of the Tunisian conservation hotspot as defined in Coll et al. 2012, to Nory El Ksabi for preparing feathers samples prior to isotopic analyses, and to Owen McFarlane for checking our English. This work would have not been possible without the permission, the human and logistics support of the Tunisian Agence de Protection et d’Aménagement du Littoral (APAL), to whom we are most grateful.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

Data collection was performed under permits from the Agence de Protection et d’Aménagement du Littoral (APAL, Permit No. 1864/12) and from the Direction des Services Vétérinaires (Permit No. 34-369).


  1. Afán I, Navarro J, Cardador L, Ramírez F, Kato A, Rodríguez B, Ropert-Coudert Y, Forero MG (2014) Foraging movements and habitat niche of two closely related seabirds breeding in sympatry. Mar Biol. doi: 10.1007/s00227-013-2368-4 Google Scholar
  2. Bearhop S, Waldron S, Votier SC, Furness RW (2002) Factors that influence assimilation rates and fractioning of nitrogen and carbon stable isotopes in avian blood and feathers. Physiol Biochem Zool 75:451–458CrossRefGoogle Scholar
  3. BirdLife International (2010) Marine important bird areas toolkit: standardised techniques for identifying priority sites for the conservation of seabirds at sea. BirdLife International, Cambridge. Version 1.2: February 2011Google Scholar
  4. Blondel J, Aronson J, Bodiou J, Boeuf G (2010) The Mediterranean region: biological diversity through time and space. Oxford University Press, OxfordGoogle Scholar
  5. Cairns DK (1989) The regulation of seabird colony size—a hinterland model. Am Nat 134:141–146. doi: 10.1086/284970 CrossRefGoogle Scholar
  6. Cardona L, Álvarez de Quevedo I, Borrell A, Aguilar A (2012) Massive consumption of gelatinous plankton by Mediterranean apex predators. PLoS ONE 7(3):e31329. doi: 10.1371/journal.pone.0031329 CrossRefGoogle Scholar
  7. 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 (Calonectris diomedea diomedea) (Aves: vertebrata) from Central Mediterranean: influence of seascape and breeding stage. Ital J Zool 80:82–89. doi: 10.1080/11250003.2012.710654 CrossRefGoogle Scholar
  8. Cherel Y, Jaquemet S, Maglio A, Jaeger A (2014) Differences in δ13C and δ15 N values between feathers and blood of seabirds chicks: implications for non-invasive isotopic investigations. Mar Biol 161:229–237. doi: 10.1007/s00227-013-2314-5 CrossRefGoogle Scholar
  9. 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. doi: 10.1007/s10021-008-9171-y CrossRefGoogle Scholar
  10. Coll M, Piroddi C, Steenbeek J, Kaschner K, Ben Rais Lasram F et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5(8):e11842. doi: 10.1371/journal.pone.0011842 CrossRefGoogle Scholar
  11. Coll M, Piroddi C, Albouy C, Ben Rais Lasram F, Cheung WWL, Christensen V et al (2012) The Mediterranean under siege: spatial overlap between marine biodiversity, cumulative threats and marine reserves. Glob Ecol Biogeogr 21:465–480. doi: 10.1111/j.1466-8238.2011.00697.x CrossRefGoogle Scholar
  12. Defos du Rau P, Bourgeois K, Ruffino L, Dromzée S, Ouni R, Abiadh A et al (2012) New assessment of the world’s largest colony of Scopoli’s Shearwater Calonectris diomedea. In: Proceedings of the 13th Medmaravis pan-Mediterranean Symposium, pp 26–28Google Scholar
  13. Delord K, Barbraud C, Bost CA, Deceuninck B, Lefebvre T, Lutz R, Micol T, Phillips RA, Trathan PN, Weimerskirch H (2014) Areas of importance for seabirds tracked from French southern territories, and recommendations for conservation. Mar Pol 48:1–13. doi: 10.1016/j.marpol.2014.02.019 CrossRefGoogle Scholar
  14. Drira Z, Belhassen M, Ayadi H, Hamza A, Zarrad R, Bouïn A, Aleya L (2010) Copepod community structure related to environmental factors from a summer cruise in the Gulf of Gabès (Tunisia, eastern Mediterranean Sea). J Mar Biol Assoc UK 90:145–157. doi: 10.1017/S0025315409990403 CrossRefGoogle Scholar
  15. Echwikhi K, Jribi I, Bradai MN, Bouaïn A (2012) Overview of loggerhead turtles coastal nets interactions in the Meditteranean Sea. Aquat Conserv 22:827–835. doi: 10.1002/aqc.2270 CrossRefGoogle Scholar
  16. Echwikhi K, Saidi B, Bradai MN, Bouaïn A (2013) Preliminary data on elasmobranch gillnet fishery in the Gulf of Gabès, Tunisia. J Appl Ichthyol 29:1080–1085. doi: 10.1111/jai.12022 CrossRefGoogle Scholar
  17. Fort J, Pettex E, Tremblay Y, Lorentsen S-H, Garthe S, Votier S, Pons J-B, Siorat F, Furness RW, Grecian JW, Bearhop S, Montevecchi WA, Grémillet D (2012) Meta-population evidence of oriented chain migration in northern gannets (Morus bassanus). Front Ecol Environ 10:237–242. doi: 10.1890/110194 CrossRefGoogle Scholar
  18. Frederiksen F, Moe B, Daunt F, Phillips RA, Barrett RT, Bogdanova MI, Boulinier T et al (2012) Multicolony tracking reveals the winter distribution of a pelagic seabird on an ocean basin scale. Div Distr 18:530–542. doi: 10.1111/j.1472-4642.2011.00864.x CrossRefGoogle Scholar
  19. Furness RW, Birkhead TR (1984) Seabird colony distributions suggest competition for food during the breeding season. Nature 311:655–656. doi: 10.1038/311655a0 CrossRefGoogle Scholar
  20. 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. 96 ppGoogle Scholar
  21. González-Solís J, Croxall JP, Oro D, Ruiz X (2007) Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Front Ecol Environ 5:297–301. doi:10.1890/1540-9295(2007)5[297:TMAMIT]2.0.CO;2CrossRefGoogle Scholar
  22. Grémillet D, Dell’Omo G, Ryan PG, Peters G, Ropert-Coudert Y, Weeks S (2004) Offshore diplomacy, or how seabirds mitigate intra-specific competition: a case study based on GPS tracking of cape gannets from neighbouring breeding sites. Mar Ecol Prog Ser 268:265–279CrossRefGoogle Scholar
  23. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Michelli F, D’Agrosa C et al (2008) A global map of human impact on marine ecosystems. Science 319:948–952. doi: 10.1126/science.1149345 CrossRefGoogle Scholar
  24. Jabeur C, Gobert B, Missaoui H (2000) Typologie de la flotilla de pêche côtière dans le golfe de Gabès (Tunisie). Aquat Liv Res 13:421–428. doi: 10.1016/S0990-7440(00)01069-X CrossRefGoogle Scholar
  25. 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. doi: 10.1111/j.1365-2656.2011.01806.x CrossRefGoogle Scholar
  26. Kelly JF (2000) Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool 78:1–27. doi: 10.1139/z99-165 CrossRefGoogle Scholar
  27. Laneri K, Louzao M, Martinez-Abran A, Arcos J, Belda E, Guallart J, Sánchez A, Giménez M, Maestre R, Oro D (2010) Trawling regime influences longline seabird bycatch in the Mediterranean: new insights from a small-scale fishery. Mar Ecol Prog Ser 420:241–252. doi: 10.3354/meps08847 CrossRefGoogle Scholar
  28. Lascelles BG, Langham GM, Ronconi RA, Reid JB (2012) From hotspots to site protection: identifying marine protected areas for seabirds around the globe. Biol Conserv 156:5–14CrossRefGoogle Scholar
  29. Le Saout S, Hoffmann M, Shi Y, Hughes A, Bernard C, Brooks TM, Bertzky B, Butchart SHM, Stuart SN, Badman T, Rodrigues ASL (2013) Protected areas and effective biodiversity conservation. Science 342:803–805. doi: 10.1126/science.1239268 CrossRefGoogle Scholar
  30. Lewis S, Sherratt TN, Hamer KC, Wanless S (2001) Evidence of intra-specific competition for food in a pelagic seabird. Nature 412:816–819. doi: 10.1038/35090566 CrossRefGoogle Scholar
  31. Lewis S, Grémillet D, Daunt F, Ryan PG, Crawford RJM, Wanless S (2006) Using behavioural variables to identify proximate causes of population change in a seabird. Oecologia 147:606–614. doi: 10.1007/s00442-005-0321-z CrossRefGoogle Scholar
  32. 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. doi: 10.3354/meps08124 CrossRefGoogle Scholar
  33. Masello JF, Mundry R, Poisbleau M, Demongin L, Voigt CC, Wikelski M, Quillfeldt P (2010) Diving seabirds share foraging space and time within and among species. Ecosphere 1(19). doi: 10.1890/ES10-00103.1
  34. 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. doi: 10.1111/j.1472-4642.2012.00916.x CrossRefGoogle Scholar
  35. Morales JM, Haydon DT, Frair J, Holsinger KE, Fryxell JM (2004) Extracting more out of relocation data: building movement models as mixtures of random walks. Ecology 85:2436–2445. doi: 10.1890/03-0269 CrossRefGoogle Scholar
  36. NOAA National Geophysical Data Center. GEODAS grid translator—design a grid.
  37. Notarbartolo-di-Sciara G, Agardy T, Hyrenbach DK, Scovazzi T, Van Klaveren P (2008) The Pelagos sanctuary for Mediterranean marine mammals. Aquat Conserv 18:367–391. doi: 10.1002/aqc.855 CrossRefGoogle Scholar
  38. Parnell A, Inger R, Bearhop S, Jackson AL (2008) SIAR: stable isotope analysis in R.
  39. Péron C, Grémillet D (2013) Tracking through life stages: adult, immature and juvenile autumn migration in a long-lived seabird. PLoS ONE 8(8):e72713. doi: 10.1371/journal.pone.0072713 CrossRefGoogle Scholar
  40. Péron C, Grémillet D (2014) Habitats marins des puffins de France métropolitaine. Agence des Aires Marines ProtégéesGoogle Scholar
  41. 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. doi: 10.1016/j.biocon.2013.09.006 CrossRefGoogle Scholar
  42. Pichegru L, Grémillet D, Crawford RJM, Ryan PG (2010) Marine no-take zone rapidly benefits endangered penguin. Biol Lett 6:498–501. doi: 10.1098/rsbl.2009.0913 CrossRefGoogle Scholar
  43. R Core Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  44. Ramos R, González-Solís J, Forero MG, Moreno R, Gómez-Díaz E, Ruiz X, Hobson KA (2009) The influence of breeding colony and sex on mercury, selenium and lead levels and carbon and nitrogen isotope signatures in summer and winter feathers of Calonectris shearwaters. Oecologia 159:345–354. doi: 10.1007/s00442-008-1215-7 CrossRefGoogle Scholar
  45. Ramos R, Granadeiro JP, Rodríguez B, Navarro J, Paiva VH, Bécares J, Reyes-González JM, Fagundes I, Ruiz A, Arcos P, González -Solís J, Catry P (2013) Meta-population feeding grounds of Cory’s shearwaters in the subtropical Atlantic ocean: implications for the definition of marine protected areas based on tracking studies. Divers Distrib 19:1284–1298. doi: 10.1111/ddi.12088 CrossRefGoogle Scholar
  46. Ruffino L, Bourgeois K, Vidal E, Duhem C, Paracuellos M, Escribano F, Sposimo P, Baccetti N, Pascal M, Oro D (2009) Invasive rats and seabirds after 2,000 years of an unwanted coexistence on Mediterranean Islands. Biol Invasions 11:1631–1651. doi: 10.1007/s10530-008-9394-z CrossRefGoogle Scholar
  47. Sangster G, Collinson JM, Crochet PA, Knox AG, Parkin DT et al (2012) Taxonomic recommendations for British birds: eighth report. Ibis 154:883. doi: 10.1111/j.1474-919X.2012.01273.x CrossRefGoogle Scholar
  48. Thiébot JB, Cherel Y, Trathan PN, Bost CA (2012) Coexistence of oceanic predators on wintering areas explained by population-scale foraging segregation in space or time. Ecology 93:122–130. doi: 10.1890/11-0385.1 CrossRefGoogle Scholar
  49. Wakefield ED, Bodey TW, Bearhop S, Blackburn J, Colhoun K, Davies R et al (2013) Space partitioning without territoriality in gannets. Science 341:68–70. doi: 10.1126/science.1236077 CrossRefGoogle Scholar
  50. Worm B, Sandow M, Oschlies A, Lotze HK, Myers RA (2005) Global patterns of predator diversity in the open oceans. Science 309:1365–1369. doi: 10.1126/science.1113399 CrossRefGoogle Scholar
  51. Zotier R, Bretagnolle V, Thibault J-C (1999) Biogeography of the marine birds of a confined sea, the Mediterranean. J Biogeogr 26:297–313CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • David Grémillet
    • 1
    • 2
    Email author
  • Clara Péron
    • 1
    • 3
  • Jean-Baptiste Pons
    • 4
  • Ridha Ouni
    • 5
  • Matthieu Authier
    • 6
  • Mathieu Thévenet
    • 7
  • Jérôme Fort
    • 8
  1. 1.CEFE-CNRS, UMR5175MontpellierFrance
  2. 2.FitzPatrick InstituteDST/NRF Excellence Centre at the University of Cape TownRondeboschSouth Africa
  3. 3.Institute for Marine and Antarctic StudiesUniversity of Tasmania and Australian Antarctic DivisionKingstonAustralia
  4. 4.Société d’Echantillonnage et d’Ingénierie Scientifique en Environnement, Le BourgIle MolèneFrance
  5. 5.Biodiversité & Ressource NaturelleTunisTunisia
  6. 6.UMS3462Observatoire PELAGISLa RochelleFrance
  7. 7.Conservatoire du LittoralAix en ProvenceFrance
  8. 8.LIENSs-CNRS-Université La RochelleLa RochelleFrance

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