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

Carreiro, Ana Rita; Paiva, Vítor H.; Medeiros, Renata; Franklin, Kirsty A.; Oliveira, Nuno; Fagundes, Ana I.; Ramos, Jaime A.

doi:10.1007/s00227-019-3626-x

Original Paper
Published: 09 January 2020

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

Ana Rita Carreiro ORCID: orcid.org/0000-0003-1300-1371¹,
Vítor H. Paiva¹,
Renata Medeiros²,
Kirsty A. Franklin³,
Nuno Oliveira⁴,
Ana I. Fagundes⁴ &
Jaime A. Ramos¹

Marine Biology volume 167, Article number: 14 (2020) Cite this article

1043 Accesses
10 Citations
18 Altmetric
Metrics details

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.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

References

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
CAS Article PubMed Google Scholar
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
Article Google Scholar
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
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. https://doi.org/10.1016/j.ecolmodel.2006.03.017
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. https://doi.org/10.1007/s00227-014-2468-9
Article Google Scholar
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
Article Google Scholar
Cunha M (1992) Análise histológica dos estados de maturaçã de verdinho (Micromesistius poutassou Risso, 1826) da costa continental portuguesa. Rel Téc Cient INIP 48:1–42
Google Scholar
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
CAS Article Google Scholar
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
Article Google Scholar
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461. https://doi.org/10.1093/bioinformatics/btq461
CAS Article PubMed Google Scholar
Edgar RC (2013) UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 10:996
CAS Article PubMed Google Scholar
Edgar RC (2016) UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing. bioRxiv. https://doi.org/10.1101/081257
Article Google Scholar
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
CAS Article PubMed Google Scholar
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
Article Google Scholar
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
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
Article Google Scholar
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
Article Google Scholar
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 299–318
Chapter Google Scholar
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 mediterranean
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
CAS Article PubMed Google Scholar
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
Article PubMed Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
CAS Article Google Scholar
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
Article Google Scholar
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
CAS Article Google Scholar
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
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
CAS 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. https://doi.org/10.1111/j.1365-2656.2011.01806.x
Article PubMed Google Scholar
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
CAS Article Google Scholar
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
Article Google Scholar
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
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 Biol Sci 269:1687–1693. https://doi.org/10.1098/rspb.2002.2083
CAS Article PubMed PubMed Central Google Scholar
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
Article Google Scholar
Libes S (2009) Introduction to marine biogeochemistry, 2nd edn. Elsevier Inc., California
Google Scholar
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
Article Google Scholar
Medeiros-Mirra R (2010) The migration strategy, diet & foraging ecology of a small seabird in a changing environment. Cardiff University, Cardiff
Google Scholar
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
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, Lisbon
Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
CAS Article PubMed PubMed Central Google Scholar
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
CAS Article Google Scholar
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, Berlengas
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
Article Google Scholar
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
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 10:19. https://doi.org/10.1371/journal.pone.0139390
CAS Article Google Scholar
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
CAS Article Google Scholar
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
CAS Article PubMed Google Scholar
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
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. https://doi.org/10.3354/meps266265
Article Google Scholar
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
Article PubMed 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. https://doi.org/10.1007/s00227-011-1725-4
Article Google Scholar
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 126:166–169
Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
R Core Team (2018) R: a language and environment for statistical computing. Computing, R Foundation for Statistical, Vienna
Google Scholar
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
Article Google Scholar
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
CAS Article Google Scholar
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
CAS Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
CAS Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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
Article Google Scholar
Stockdale JE (2018) Using high-throughput sequencing to track habitat use by thrushes exploiting heterogeneous farmland landscapes. Cardiff University, Cardiff
Google Scholar
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
CAS Article PubMed Google Scholar
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
CAS Article Google Scholar
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
Article PubMed Google Scholar
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
CAS Article Google Scholar
Warham J (1990) The petrels: their ecology and breeding systems. Academic Press, London
Google Scholar
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
Article Google Scholar
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
Article Google Scholar
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 39:129–134
Google Scholar
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
Article Google Scholar
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
CAS Article PubMed Google Scholar
Zhang Z, Schwartz S, Wagner L, Mille W (2000) A greedy algorithm for aligning DNA sequences. J Comput Biol 7:203–214
CAS Article PubMed Google Scholar

Download references

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).

Author information

Authors and Affiliations

Department of Life Sciences, MARE, Marine and Environmental Sciences Centre, University of Coimbra, 3004-517, Coimbra, Portugal
Ana Rita Carreiro, Vítor H. Paiva & Jaime A. Ramos
Cardiff School of Dentistry, Cardiff University, Heath Park, Academic Av., Cardiff, CF14 4XY, UK
Renata Medeiros
School of Biological Sciences, University of East Anglia, Norwich Research Park, Norwich, UK
Kirsty A. Franklin
Sociedade Portuguesa para o Estudo das Aves, Av. Columbano Bordalo Pinheiro 87, 1070-062, Lisbon, Portugal
Nuno Oliveira & Ana I. Fagundes

Authors

Ana Rita Carreiro
View author publications
You can also search for this author in PubMed Google Scholar
Vítor H. Paiva
View author publications
You can also search for this author in PubMed Google Scholar
Renata Medeiros
View author publications
You can also search for this author in PubMed Google Scholar
Kirsty A. Franklin
View author publications
You can also search for this author in PubMed Google Scholar
Nuno Oliveira
View author publications
You can also search for this author in PubMed Google Scholar
Ana I. Fagundes
View author publications
You can also search for this author in PubMed Google Scholar
Jaime A. Ramos
View author publications
You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana Rita Carreiro.

Ethics declarations

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.

Additional information

Publisher's Note

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

Reviewed by Undisclosed experts.

Responsible Editor: Y. Cherel.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 72 kb)

Supplementary material 2 (PDF 138 kb)

Supplementary material 3 (PDF 100 kb)

Supplementary material 4 (PDF 155 kb)

Supplementary material 5 (PDF 153 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Carreiro, A.R., Paiva, V.H., Medeiros, R. et al. Metabarcoding, stables isotopes, and tracking: unraveling the trophic ecology of a winter-breeding storm petrel (Hydrobates castro) with a multimethod approach. Mar Biol 167, 14 (2020). https://doi.org/10.1007/s00227-019-3626-x

Download citation

Received: 06 February 2019
Accepted: 15 November 2019
Published: 09 January 2020
DOI: https://doi.org/10.1007/s00227-019-3626-x