Advertisement

Marine Biology

, 167:14 | Cite as

Metabarcoding, stables isotopes, and tracking: unraveling the trophic ecology of a winter-breeding storm petrel (Hydrobates castro) with a multimethod approach

  • Ana Rita CarreiroEmail author
  • Vítor H. Paiva
  • Renata Medeiros
  • Kirsty A. Franklin
  • Nuno Oliveira
  • Ana I. Fagundes
  • Jaime A. Ramos
Original Paper

Abstract

Detailed information on diet and foraging ecology is scarce for most small seabirds such as storm petrels. In this study, we used molecular techniques, stable isotope analysis, and geolocators to study the diet, trophic ecology, and at-sea distribution of Madeiran storm petrels (Hydrobates castro) breeding in Farilhões Islet, Portugal, in 2015–2017. The diet of Madeiran storm petrels was dominated by fish for both sexes and study years, with Gadidae representing the main prey family. In 2017, females also fed on Aulopiformes, Stomiiformes and Myctophiformes, which were not identified in the other groups, suggesting some degree of inter-annual and intersexual plasticity in their diet. The carbon isotopic ratios of birds during 2017 were significantly higher when compared to 2015, which might be related to foraging near coastal areas in 2017. Indeed, tracking data for 2017 show that birds foraged near the colony and near the West African coast. Overall, both sexes of this species exhibited a similar trophic ecology and diet during the breeding season. However, intersexual differences occurred during the non-breeding season, when females showed significantly lower nitrogen isotopic ratios than males (in 2016), and the lowest niche overlap between sexes occurred. This, together with the fact that environmental conditions appeared less favourable in 2016 suggests that intersexual differences in the foraging ecology of this species may be related with environmental conditions.

Notes

Acknowledgements

To all volunteers and colleagues who collaborate during the fieldwork. To Berlengas Natural Reserve—Portuguese Institute for Nature Conservation and Forests and the Portuguese Maritime Authority by provide transport and accommodation from Peniche to Farilhão Islet. To captaincy of Peniche and RNB-ICNF. We thank the reviewers that contributed significantly to the improvement of the manuscript.

Funding

Fieldwork financial support was provided by project LIFE13 NAT/PT/000458 co-funded by the LIFE Program of European Commission and Fundo Ambiental grant from the Portuguese Government. This research was co-sponsored by the Foundation for Science and Technology (FCT; Portugal) and the European Social Fund (POPH,EU) through post-doctoral grants to V.H.P. (SFRH/BPD/85024/2012) and the strategic program of MARE (MARE—UID/MAR/04292/2019).

Compliance with ethical standards

Conflict of interest

All authors declare that they have no conflict of interests.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All animal handling and procedures in this research were duly approved and licensed by permits from the Portuguese Institute for Nature Conservation and Forests (Licenses number 174/2015, 8/2016, 177/2016 and 494/2016/CAPT), which follow the European Union Directive on the protection of animals used for scientific purposes (Directive 2010/63/EU) and Portuguese laws No. 140/99, No. 49/2005, No. 316/89, and No. 180/2008. Documentary evidence available under request.

Supplementary material

227_2019_3626_MOESM1_ESM.pdf (72 kb)
Supplementary material 1 (PDF 72 kb)
227_2019_3626_MOESM2_ESM.pdf (138 kb)
Supplementary material 2 (PDF 138 kb)
227_2019_3626_MOESM3_ESM.pdf (101 kb)
Supplementary material 3 (PDF 100 kb)
227_2019_3626_MOESM4_ESM.pdf (155 kb)
Supplementary material 4 (PDF 155 kb)
227_2019_3626_MOESM5_ESM.pdf (154 kb)
Supplementary material 5 (PDF 153 kb)

References

  1. Bachy C, Dolan JR, López-García P, Deschamps P, Moreira D (2013) Accuracy of protist diversity assessments: morphology compared with cloning and direct pyrosequencing of 18S rRNA genes and ITS regions using the conspicuous tintinnid ciliates as a case study. ISME J 7:244–255.  https://doi.org/10.1038/ismej.2012.106 CrossRefPubMedGoogle Scholar
  2. Blackmer AL, Ackerman JT, Nevitt GA (2004) Effects of investigator disturbance on hatching success and nest-site fidelity in a long-lived seabird, Leach’s storm-petrel. Biol Conserv 116:141–148.  https://doi.org/10.1016/S0006-3207(03)00185-X CrossRefGoogle Scholar
  3. Bolton M, Smith AL, Gomez-Diaz E, Friesen VL, Medeiros R, Bried J, Roscales JL, Furness RW (2008) Monteiro’s Storm-petrel Oceanodroma monteiroi: a new species from the Azores. Ibis (Lond 1859) 150:717–727.  https://doi.org/10.1111/j.1474-919x.2008.00854.x CrossRefGoogle Scholar
  4. 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.  https://doi.org/10.1016/j.ecolmodel.2006.03.017 CrossRefGoogle Scholar
  5. 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.  https://doi.org/10.1007/s00227-014-2468-9 CrossRefGoogle Scholar
  6. Ceia FR, Cherel Y, Paiva VH, Ramos JA (2018) Stable isotope dynamics (δ13C and δ15N) in neritic and oceanic waters of the north atlantic inferred from GPS-tracked Cory’s shearwaters. Front Mar Sci.  https://doi.org/10.3389/fmars.2018.00377 CrossRefGoogle Scholar
  7. Cunha M (1992) Análise histológica dos estados de maturaçã de verdinho (Micromesistius poutassou Risso, 1826) da costa continental portuguesa. Rel Téc Cient INIP 48:1–42Google Scholar
  8. Deagle BE, Gales NJ, Evans K, Jarman SN, Robinson S, Trebilco R, Hindell MA (2007) Studying seabird diet through genetic analysis of faeces: a case study on Macaroni Penguins (Eudyptes chrysolophus). PLoS One 2:10.  https://doi.org/10.1371/journal.pone.0000831 CrossRefGoogle Scholar
  9. Deagle BE, Chiaradia A, McInnes J, Jarman SN (2010) Pyrosequencing faecal DNA to determine diet of little penguins: is what goes in what comes out? Conserv Genet 11:2039–2048.  https://doi.org/10.1007/s10592-010-0096-6 CrossRefGoogle Scholar
  10. Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461.  https://doi.org/10.1093/bioinformatics/btq461 CrossRefPubMedGoogle Scholar
  11. Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996CrossRefGoogle Scholar
  12. Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv.  https://doi.org/10.1101/081257 CrossRefGoogle Scholar
  13. Edgar RC, Flyvbjerg H (2015) Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics 31:3476–3482.  https://doi.org/10.1093/bioinformatics/btv401 CrossRefPubMedGoogle Scholar
  14. Elliott KH, Gaston AJ, Crump D (2010) Sex-specific behavior by a monomorphic seabird represents risk partitioning. Behav Ecol 21:1024–1032.  https://doi.org/10.1093/beheco/arq076 CrossRefGoogle Scholar
  15. Forero MG, Hobson KA (2003) Using stable isotopes of nitrogen and carbon to study seabird ecology: applications in the Mediterranean seabird community. Sci Mar 67:23–32.  https://doi.org/10.3989/scimar.2003.67s223 CrossRefGoogle Scholar
  16. Gladbach A, McGill RAR, Quillfeldt P (2007) Foraging areas of Wilson’s storm-petrel Oceanites oceanicus in the breeding and inter-breeding period determined by stable isotope analysis. Polar Biol 30:1005–1012.  https://doi.org/10.1007/s00300-007-0258-2 CrossRefGoogle Scholar
  17. González-Solís J, Croxall JP, Wood AG (2000) Sexual dimorphism and sexual segregation in foraging strategies of northern giant petrels, Macronectes halli, during incubation. Oikos 90:390–398.  https://doi.org/10.1034/j.1600-0706.2000.900220.x CrossRefGoogle Scholar
  18. 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. Isoscapes. Springer Netherlands, Dordrecht, pp 299–318CrossRefGoogle Scholar
  19. Granadeiro JP, Grade N, Lecoq M, Morais L, Santos C, Silva MC (1998a) Breeding Madeiran Storm-petrels Oceanodroma castro on the Farilhões islands, Portugal. In: Proceedings of the IV mediterranean seabird symposium: seabird ecology and coastal zone management in the mediterraneanGoogle Scholar
  20. Granadeiro JP, Nunes M, Silva MC, Furness RW (1998b) Flexible foraging strategy of Cory’s shearwater, Calonectris diomedea, during the chick-rearing period. Anim Behav 56:1169–1176.  https://doi.org/10.1006/anbe.1998.0827 CrossRefPubMedGoogle Scholar
  21. Gremillet D, Charmantier A (2010) Shifts in phenotypic plasticity constrain the value of seabirds as ecological indicators of marine ecosystems. Ecol Appl 20:1498–1503.  https://doi.org/10.1890/09-1586.1 CrossRefPubMedGoogle Scholar
  22. Grémillet D, Fort J, Amélineau F, Zakharova E, Le Bot T, Sala E, Gavrilo M (2015) Arctic warming: nonlinear impacts of sea-ice and glacier melt on seabird foraging. Glob Change Biol 21:1116–1123.  https://doi.org/10.1111/gcb.12811 CrossRefGoogle Scholar
  23. Halpin LR, Pollet IL, Lee C, Morgan KH, Carter HR (2018) Year-round movements of sympatric Fork-tailed (Oceanodroma furcata) and Leach’s (O. leucorhoa) storm-petrels. J Field Ornithol 89:207–220.  https://doi.org/10.1111/jofo.12255 CrossRefGoogle Scholar
  24. Hedd A, Montevecchi WA (2006) Diet and trophic position of Leach’s storm-petrel Oceanodroma leucorhoa during breeding and moult, inferred from stable isotope analysis of feathers. Mar Ecol Prog Ser 322:291–301.  https://doi.org/10.3354/meps322291 CrossRefGoogle Scholar
  25. Hedd A, Fifield DA, Burke CM, Montevecchi WA, Tranquilla LM, Regular PM, Buren AD, Robertson GJ (2010) Seasonal shift in the foraging niche of Atlantic puffins Fratercula arctica revealed by stable isotope (δ15 N and δ13C) analyses. Aquat Biol 9:13–22.  https://doi.org/10.3354/ab00225 CrossRefGoogle Scholar
  26. Horswill C, Jackson JA, Medeiros R, Nowell RW, Trathan PN, O’Connell TC (2018) Minimising the limitations of using dietary analysis to assess foodweb changes by combining multiple techniques. Ecol Indic 94:218–225.  https://doi.org/10.1016/j.ecolind.2018.06.035 CrossRefGoogle Scholar
  27. Hurrell J (2017) The climate data guide: Hurrell North Atlantic Oscillation (NAO) Index (station-based). https://climatedataguide.ucar.edu/climate-data/hurrell-north-atlantic-oscillation-nao-index-station-based. Accessed 17 Mar 2017
  28. Iverson SJ, Springer AM, Kitaysky AS (2007) Seabirds as indicators of food web structure and ecosystem variability: qualitative and quantitative diet analyses using fatty acids. Mar Ecol Prog Ser 352:235–244.  https://doi.org/10.3354/meps07073 CrossRefGoogle Scholar
  29. 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.  https://doi.org/10.1111/j.1365-2656.2011.01806.x CrossRefGoogle Scholar
  30. Jarman SN, McInnes JC, Faux C, Polanowski AM, Marthick J, Deagle BE, Southwell C, Emmerson L (2013) Adelie penguin population diet monitoring by analysis of food DNA in scats. PLoS One 8:11.  https://doi.org/10.1371/journal.pone.0082227 CrossRefGoogle Scholar
  31. Kato A, Watanuki Y, Nishumi I, Kuroki M, Shaugnessy P, Naito Y (2000) Variation in foraging and parental behavior of King cormorants. Auk 117:718–730.  https://doi.org/10.1642/0004-8038(2000)117%5b0718:VIFAPB%5d2.0.CO;2 CrossRefGoogle Scholar
  32. Kürten N, Vedder O, González J, Heiko S, Bouwhuis S (2019) No detectable effect of light-level geolocators on the behaviour and fitness of a long-distance migratory seabird. J Ornithol.  https://doi.org/10.1007/s10336-019-01686-3 CrossRefGoogle Scholar
  33. 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 Biol Sci 269:1687–1693.  https://doi.org/10.1098/rspb.2002.2083 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Lewis S, Schreiber EA, Daunt F, Schenk GA, Orr K, Adams A, Wanless S, Hamer KC (2005) Sex-specific foraging behaviour in tropical boobies: does size matter? Ibis (Lond 1859) 147:408–414.  https://doi.org/10.1111/j.1474-919x.2005.00428.x CrossRefGoogle Scholar
  35. Libes S (2009) Introduction to marine biogeochemistry, 2nd edn. Elsevier Inc., CaliforniaGoogle Scholar
  36. Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10.  https://doi.org/10.14806/ej.17.1.200 CrossRefGoogle Scholar
  37. Medeiros-Mirra R (2010) The migration strategy, diet & foraging ecology of a small seabird in a changing environment. Cardiff University, CardiffGoogle Scholar
  38. Meirinho A, Barros N, Oliveira N, Catry P, Lecoq M, Geraldes P, Granadeiro JP, Ramírez I, Andrade J (2014) Atlas das Aves Marinhas de Portugal. http://www.atlasavesmarinhas.pt. Accessed 17 Mar 2015
  39. Mendes ARN (2013) Status and conservation of Madeiran Storm-petrel Oceanodroma castro in Farilhão Grande, Berlengas, Portugal: relevance to the management plan of this protected area. Universidade de Lisboa, LisbonGoogle Scholar
  40. Monteiro LR, Furness RW (1998) Speciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? Philos Trans R Soc London Ser B Biol Sci 353:945–953.  https://doi.org/10.1098/rstb.1998.0259 CrossRefGoogle Scholar
  41. Monteiro LR, Ramos JA, Furness RW, del Nevo AJ (1996a) Movements, morphology, breeding, moult, diet and feeding of seabirds in the Azores. Colon Waterbirds 19:82–97.  https://doi.org/10.2307/1521810 CrossRefGoogle Scholar
  42. Monteiro LR, Ramos JA, Furness RW (1996b) Past and present status and conservation of the seabirds breeding in the Azores Archipelago. Biol Conserv 78:319–328.  https://doi.org/10.1016/s0006-3207(96)00037-7 CrossRefGoogle Scholar
  43. Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schäffer AA (2008) Database indexing for production MegaBLAST searches. Bioinformatics 24:1757–1764.  https://doi.org/10.1093/bioinformatics/btn322 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Nürnberg D, Ziegler M, Karas C, Tiedemann R, Schmidt MW (2008) Interacting loop current variability and Mississippi River discharge over the past 400 kyr. Earth Planet Sci Lett 272:278–289.  https://doi.org/10.1016/j.epsl.2008.04.051 CrossRefGoogle Scholar
  45. Oliveira N, Mendes AR, Geraldes P, Barros N, Andrade J, Ramírez I (2013) Monitorização da população reprodutora de Roque-de-castro Oceanodroma castro do Farilhão Grande, BerlengasGoogle Scholar
  46. Paiva VH, Xavier J, Geraldes P, Ramirez I, Garthe S (2010a) Foraging ecology of Cory’ s shearwaters in different oceanic environments of the North Atlantic. Mar Ecol Prog Ser.  https://doi.org/10.3354/meps08617 CrossRefGoogle Scholar
  47. Paiva VH, Geraldes P, Ramírez I, Meirinho A, Garthe S, Ramos JA (2010b) Oceanographic characteristics of areas used by Cory’s shearwaters during short and long foraging trips in the North Atlantic. Mar Biol 157:1385–1399.  https://doi.org/10.1007/s00227-010-1417-5 CrossRefGoogle Scholar
  48. 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 10:19.  https://doi.org/10.1371/journal.pone.0139390 CrossRefGoogle Scholar
  49. Paiva VH, Fagundes AI, Romão V, Gouveia C, Ramos JA (2016) Population-scale foraging segregation in an apex predator of the north Atlantic. PLoS One 11:1–19.  https://doi.org/10.1371/journal.pone.0151340 CrossRefGoogle Scholar
  50. Paiva VH, Ramos JA, Nava C, Neves V, Bried J, Magalhães M (2018) Inter-sexual habitat and isotopic niche segregation of the endangered Monteiro’s storm-petrel during breeding. Zoology 126:29–35.  https://doi.org/10.1016/j.zool.2017.12.006 CrossRefPubMedGoogle Scholar
  51. Peck DR, Congdon BC (2006) Sex-specific chick provisioning and diving behaviour in the wedge-tailed shearwater Puffinus pacificus. J Avian Biol 37:245–251.  https://doi.org/10.1111/j.2006.0908-8857.03558.x CrossRefGoogle Scholar
  52. 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.  https://doi.org/10.3354/meps266265 CrossRefGoogle Scholar
  53. Phillips RA, Bearhop S, McGill RAR, Dawson DA (2009) Stable isotopes reveal individual variation in migration strategies and habitat preferences in a suite of seabirds during the nonbreeding period. Oecologia 160:795–806.  https://doi.org/10.1007/s00442-009-1342-9 CrossRefPubMedGoogle Scholar
  54. 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.  https://doi.org/10.1007/s00227-011-1725-4 CrossRefGoogle Scholar
  55. Pollet IL, Lancaster MB, Lightfoot HL, Vaasjo EJ, Shutler D (2014a) Fifty one degrees and 14 years of separation: a trans-atlantic recapture of a banded Leach’s storm-petrel. Wilson J Ornithol 126:166–169CrossRefGoogle Scholar
  56. Pollet IL, Ronconi RA, Jonsen ID, Leonard ML, Taylor PD, Shutler D (2014b) Foraging movements of Leach’s storm-petrels Oceanodroma leucorhoa during incubation. J Avian Biol 45:305–314.  https://doi.org/10.1111/jav.00361 CrossRefGoogle Scholar
  57. Pollet IL, Hedd A, Taylor PD, Montevecchi WA, Shutler D (2014c) Migratory movements and wintering areas of Leach’s Storm-Petrels tracked using geolocators. J Field Ornithol 85:321–328.  https://doi.org/10.1111/jofo.12071 CrossRefGoogle Scholar
  58. R Core Team (2018) R: a language and environment for statistical computing. Computing, R Foundation for Statistical, ViennaGoogle Scholar
  59. Ramos R, González-Solís J (2012) Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front Ecol Environ 10:258–266.  https://doi.org/10.1890/110140 CrossRefGoogle Scholar
  60. Ramos R, Gonzalez-Solis J, Croxall JP, Oro D, Ruiz X (2009) Understanding oceanic migrations with intrinsic biogeochemical markers. PLoS One 4:6.  https://doi.org/10.1371/journal.pone.0006236 CrossRefGoogle Scholar
  61. Ramos JA, Isabel Fagundes A, 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 Res Part I Oceanogr Res Pap 104:60–71.  https://doi.org/10.1016/j.dsr.2015.07.001 CrossRefGoogle Scholar
  62. Robinson CJ (2004) Responses of the northern anchovy to the dynamics of the pelagic environment: identification of fish behaviours that may leave the population under risk of overexploitation. J Fish Biol 64:1072–1087.  https://doi.org/10.1111/j.1095-8649.2004.00372.x CrossRefGoogle Scholar
  63. Rodway MS, Montevecchi WA, Chardine JW (1996) Effects of investigator disturbance on breeding success of Atlantic puffins Fratercula arctica. Biol Conserv 76:311–319.  https://doi.org/10.1016/0006-3207(94)00118-9 CrossRefGoogle Scholar
  64. Rogers SI, Rijnsdorp AD, Damm U, Vanhee W (1998) Demersal fish populations in the coastal waters of the UK and continental NW Europe from beam trawl survey data collected from 1990 to 1995. J Sea Res 39:79–102.  https://doi.org/10.1016/S1385-1101(97)00021-X CrossRefGoogle Scholar
  65. Roscales JL, Gomez-Diaz E, Neves V, Gonzalez-Solis J (2011) Trophic versus geographic structure in stable isotope signatures of pelagic seabirds breeding in the northeast Atlantic. Mar Ecol Prog Ser 434:1–13.  https://doi.org/10.3354/meps09211 CrossRefGoogle Scholar
  66. Santos AMP, Peliz A, Dubert J, Oliveira PB, Angélico MM, Ré P (2004) Impact of a winter upwelling event on the distribution and transport of sardine (Sardina pilchardus) eggs and larvae off western Iberia: a retention mechanism. Cont Shelf Res 24:149–165.  https://doi.org/10.1016/j.csr.2003.10.004 CrossRefGoogle Scholar
  67. Sousa FM, Nascimento S, Casimiro H, Boutov D (2008) Identification of upwelling areas on sea surface temperature images using fuzzy clustering. Remote Sens Environ 112:2817–2823.  https://doi.org/10.1016/j.rse.2008.01.014 CrossRefGoogle Scholar
  68. Springer AM, Roseneau DG, Murphy EC, Springer MI (1984) Environmental controls of marine food webs—food-habits of seabirds in the Eastern Chukchi Sea. Can J Fish Aquat Sci 41:1202–1215.  https://doi.org/10.1139/f84-142 CrossRefGoogle Scholar
  69. Stockdale JE (2018) Using high-throughput sequencing to track habitat use by thrushes exploiting heterogeneous farmland landscapes. Cardiff University, CardiffGoogle Scholar
  70. Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641.  https://doi.org/10.1046/j.1365-294X.2002.01471.x CrossRefPubMedGoogle Scholar
  71. Traugott M, Pázmándi C, Kaufmann R, Juen A (2007) Evaluating 15N/14N and 13C/12C isotope ratio analysis to investigate trophic relationships of elaterid larvae (Coleoptera: Elateridae). Soil Biol Biochem 39:1023–1030.  https://doi.org/10.1016/j.soilbio.2006.11.012 CrossRefGoogle Scholar
  72. Valentini A, Pompanon F, Taberlet P (2009) DNA barcoding for ecologists. Trends Ecol Evol 24:110–117.  https://doi.org/10.1016/j.tree.2008.09.011 CrossRefPubMedGoogle Scholar
  73. Wada E (2009) Stable δ15N and δ13C isotope ratios in aquatic ecosystems. Proc Jpn Acad Ser B 85:98–107.  https://doi.org/10.2183/pjab/85.98 CrossRefGoogle Scholar
  74. Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, LondonGoogle Scholar
  75. Weimerskirch H (1998) How can a pelagic seabird provision its chick when relying on a distant food resource? Cyclic attendance at the colony, foraging decision and body condition in sooty shearwaters. J Anim Ecol 67:99–109.  https://doi.org/10.1046/j.1365-2656.1998.00180.x CrossRefGoogle Scholar
  76. Welcker J, Steen H, Harding AMA, Gabrielsen GW (2009) Sex-specific provisioning behaviour in a monomorphic seabird with a bimodal foraging strategy. Ibis (Lond 1859) 151:502–513.  https://doi.org/10.1111/j.1474-919x.2009.00931.x CrossRefGoogle Scholar
  77. Xavier JC, Magalhães MC, Mendonça AS, Antunes M, Carvalho N, Machete M, Santos RS, Paiva V, Hamer KC (2011) Changes in diet of Cory’s Shearwaters Calonectris diomedea breeding in the Azores. Mar Ornitol 39:129–134Google Scholar
  78. Xavier JC, Cherel Y, Medeiros R, Velez N, Dewar M, Ratcliffe N, Carreiro AR, Trathan PN (2018) Conventional and molecular analysis of the diet of gentoo penguins: contributions to assess scats for non-invasive penguin diet monitoring. Polar Biol.  https://doi.org/10.1007/s00300-018-2364-8 CrossRefGoogle Scholar
  79. Zeale M, Butlin R, Barker G, Lees D, Jones G (2011) Taxon-specific PCR for DNA barcoding arthropod prey in bat faeces. Mol Ecol Resour 11:236–244.  https://doi.org/10.1111/j.1755-0998.2010.02920.x CrossRefPubMedGoogle Scholar
  80. Zhang Z, Schwartz S, Wagner L, Mille W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Life Sciences, MARE, Marine and Environmental Sciences CentreUniversity of CoimbraCoimbraPortugal
  2. 2.Cardiff School of DentistryCardiff University, Heath ParkCardiffUK
  3. 3.School of Biological SciencesUniversity of East AngliaNorwichUK
  4. 4.Sociedade Portuguesa para o Estudo das AvesLisbonPortugal

Personalised recommendations