Skip to main content
Log in

The importance of Portuguese Continental Shelf Waters to Balearic Shearwaters revealed by aerial census

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The Balearic shearwater Puffinus mauretanicus is one of the most threatened seabirds in the world. To evaluate the abundance and distribution of Balearic Shearwaters in Portuguese Continental Shelf Waters, during the post-breeding period when migrating birds are outside the Mediterranean Sea, we conducted 5 aerial surveys between 2010 and 2014 (21 survey days covering 62,716 km2). Following a line transect method, observers recorded a total of 181 Balearic Shearwaters sightings. Using Distance sampling software, we estimated an overall species abundance (2010–2014) of 10,182, ranging between 2338 in 2010 and 23,221 individuals in 2012. During the 2012 post-breeding period, the Portuguese Continental Shelf Waters were used by up to 96.8% of the latest migratory population assessment. Considering Balearic Shearwater estimates per sampling block, there was a preference for the North and Center sectors of the Portuguese coast (respectively, 7058 and 1366 individuals) where several SPAs were already designated. We computed the annual and overall habitat predictive models for Balearic Shearwaters using a maximum entropy algorithm on MaxEnt software. In all models, the Balearic shearwater distribution was best predicted by mean chlorophyll concentration. Balearic Shearwaters are mostly present in shallow shelf and coastal waters particularly in the widest portions of the continental shelf. These areas are strongly influenced by upwelling, which concurs with the chlorophyll concentration being the most important predicting variable. Portuguese Continental Shelf Waters are one of the most important post-breeding grounds to the Balearic Shearwater.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abelló P, Esteban A (2012) Trawling bycatch dos affect Balearic Shearwaters Puffinus mauretanicus. Rev Catalana Ornitol 28:34–39

    Google Scholar 

  • 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 161:657–668. doi:10.1007/s00227-013-2368-4

    Article  Google Scholar 

  • Ainley DG, Ribic CA, Woehler EJ (2012) Adding the ocean to the study of seabirds: A brief history of at-sea seabird research. Mar Ecol Prog Ser 451:231–243. doi:10.3354/meps09524

    Article  Google Scholar 

  • Arcos JM (2011a) International species action plan for the Balearic shearwater, Puffinus mauretanicus. SEO/BirdLife and BirdLife International (compiler)

  • Arcos JM (2011b) Cuantas pardelas baleares hay? Discrepancias entre los censos en colonias y en el mar. In: Valeiras X, Muñoz G, Bermejo A, Arcos JM, Paterson AM (ed) Actas del 6° Congreso del GIAM y el Taller internacional sobre la Ecología de Paiños y Pardelas en el sur de Europa. Boletín del Grupo Ibérico de Aves Marinas, pp 117–121

  • Arroyo GM, Mateos-Rodríguez M, Muñoz AR, De La Cruz A, Cuenca D, Onrubia A (2014) New population estimates of a critically endangered species, the Balearic Shearwater Puffinus mauretanicus, based on coastal migration counts. Bird Conserv Int 26:87–99. doi:10.1017/S095927091400032X

    Article  Google Scholar 

  • BirdLife International (2015) Puffinus mauretanicus. The IUCN Red List of Threatened Species. e.T22728432A82342251. doi:10.2305/IUCN.UK.2015-4.RLTS.T22728432A82342251.en (downloaded on 12 September 2016)

  • Boué A, Louzao M, Arcos JM, Delord K, Weimerskirch H, Cortes V, Barros N, Guilford T, Arroyo GM, Oro D, Andrade J, Garcia D, Dalloyau S, Gonzalez-Solis J, Newton S, Wynn R, Micol T (2013) First Meeting of the Population and Conservation Status Working Group. Recent and current research on Balearic shearwater on colonies and in Atlantic and Mediterranean areas. Agreement on the Conservation of Albatrosses and Petrels, La Rochelle

    Google Scholar 

  • Bretagnolle V, Certain G, Houte S, Métais M (2004) Distribution maps and minimum abundance estimates for wintering auks in the Bay of Biscay, based on aerial surveys. Aquat Living Resour 17:353–360. doi:10.1051/alr:2004044

    Article  Google Scholar 

  • Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers DL, Thomas L (2001) Introduction to distance sampling: estimating abundance of biological populations. Oxford University Press, London

    Google Scholar 

  • Buckland ST, Marsden SJ, Green RE (2008) Estimating bird abundance: making methods work. Bird Conserv Int 18:S91–S108

    Article  Google Scholar 

  • Buckland ST, Burt LM, Rexstad EA, Mellor M, Williams AE, Woodward R (2012) Aerial surveys of seabirds: the advent of digital methods. J Appl Ecol 49:960–967. doi:10.1111/j.1365-2664.2012.02150.x

    Article  Google Scholar 

  • Camphuysen CJ, Fox AD, Leopold MF, Petersen IK (2004) Towards standardised seabirds at sea census techniques in connection with environmental impact assessments for offshore wind farms in the UK Report No. BAM-02-2002. COWRIE, London

    Google Scholar 

  • Certain G, Bretagnolle V (2008) Monitoring seabirds population in marine ecosystem: the use of strip-transect aerial surveys. Remote Sens Environ 112:3314–3322. doi:10.1016/j.rse.2008.01.019

    Article  Google Scholar 

  • Cooper J, Baccetti N, Belda EJ, Borg JJ, Oro D, Papaconstantinou C, Sánchez A (2003) Seabird mortality from longline fishing in the Mediterranean Sea and Macaronesian waters: a review and a way forward. Sci Mar 67:57–64. doi:10.3989/scimar.2003.67s257

    Article  Google Scholar 

  • Costa RA, Torres J, Vingada JV, Eira C (2016) Persistent organic pollutants and inorganic elements in the Balearic shearwater (Puffinus mauretanicus) wintering off Portugal. Mar Pollut Bull 108:311–316. doi:10.1016/j.marpolbul.2016.04.039

    Article  CAS  Google Scholar 

  • Cunningham GB, Nevitt GA (2005) The sense of smell in procellariiforms: An overview and new directions. In: Mason RT, LeMaster MP, Müller-Schwarze D (eds) Chemical Signals in Vertebrates, vol 10, pp 403–408. doi:10.1007/0-387-25160-X_47

  • Darlaston M, Wynn RB (2012) A record influx of Balearic shearwaters in Devon and Cornwall. Br Birds 105:37–38

    Google Scholar 

  • Davoren GK, Montevecchi WA, Anderson JT (2003a) Search strategies of a pursuit-diving marine bird and the persistence of prey patches. Ecol Monogr 73:463–481

    Article  Google Scholar 

  • Davoren GK, Montevecchi WA, Anderson JT (2003b) Distributional patterns of a marine bird and its prey: habitat selection based on prey and conspecific behaviour. Mar Ecol Prog Ser 256:229–242. doi:10.3354/meps256229

    Article  Google Scholar 

  • Elith JH, Graham CP, Anderson R, Dudik M, Ferrier S, Guisan A, Hijmans RJ, Huettmann FR, Leathwick J, Lehmann A, Li JG, Lohmann LA, Loiselle B, Manion G, Moritz C, Nakamura M, Nakazawa Y, Overton M, Peterson AT, Phillips SJ, Zimmerman N (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151. doi:10.1111/j.2006.0906-7590.04596.x

    Article  Google Scholar 

  • Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Diversity Distrib 17:43–57. doi:10.1111/j.1472-4642.2010.00725.x

    Article  Google Scholar 

  • Février Y, Plestan M, Thébault L, Hémery F, Denjau A, Sturbois A (2011) Stationnement du puffin des Baléares Puffinus mauretanicus en Côtes-d’Armor en 2010. Le Fou 83:39–48

    Google Scholar 

  • Fiúza AFG (1983) Upwelling patterns off Portugal. In: Suess E, Thiede J (eds) Coastal upwelling its sediment record. Springer, New York, pp 85–98

    Chapter  Google Scholar 

  • Genovart M, Arcos JM, Álvarez D, McMinn M, Meier R, Wynn RB, Guilford T, Oro D (2016) Demography of the critically endangered Balearic shearwater: the impact of fisheries and time to extinction. J Appl Ecol 53:1158–1168. doi:10.1111/1365-2664.12622

    Article  Google Scholar 

  • Guilford T, Wynn R, McMinn M, Rodríguez A, Fayet A, Maurice L, Jones A, Meier R (2012) Geolocators reveal migration and pre-breeding behaviour of the critically endangered Balearic Shearwater Puffinus mauretanicus. PLoS One 7(3):e33753. doi:10.1371/journal.pone.0033753

    Article  CAS  Google Scholar 

  • Hyrenbach KD, Veit RR, Weimerskirch H, Metzl N, Hunt Jr GL (2007) Community structure across a large-scale ocean productivity gradient: Marine bird assemblages of the Southern Indian Ocean. Deep-Sea Res PT I 54:1129–1145. doi:10.1016/j.dsr.2007.05.002

  • ICNF (2014) Proposta técnica de Zonas de Protecção Especial no meio marinho a designar em Portugal continental. http://www.icnf.pt/portal/icnf/participacao-publica/resource/zpe/ZPE_meio_marinho_participacao_publica.pdf (05 February 2016)

  • Jones AR, Wynn RB, Yésou P, Thébault L Collins P, Suberg L, Lewis KM, Brereton TM (2014) Using integrated land- and boat-based surveys to inform conservation of the Critically Endangered Balearic shearwater. Endang Species Res 25:1–18.doi:10.3354/esr00611

    Article  Google Scholar 

  • Kumar S, Stohlgren TJ (2009) MaxEnt modeling for predicting suitable habitat for threatened and endangered tree Canacomyrica monticola in New Caledonia. J Ecol Nat Environ 1:94–98

    Google Scholar 

  • Le Corre M, Jaeger A, Pinet P, Kappes MA, Weimerskirch H, Catry T, Ramos J, Russel J, Shah N, Jaquemet S (2012) Tracking seabirds to identify potential Marine Protected Areas in the tropical western Indian Ocean. Biol Conserv 156:83–93

    Article  Google Scholar 

  • Lieske DJ, Fifield DA, Gjerdrum C (2014) Maps, models, and marine vulnerability: assessing the community distribution of seabirds at-sea. Biol Conserv 172:15–28. doi:10.1016/j.biocon.2014.02.010

    Article  Google Scholar 

  • Louzao M, Hyrenbach KD, Arcos JM, Abelló P, Gil de Sola L, Oro D (2006) Oceanographic habitat of an endangered Mediterranean procellariiform: implications for marine protected areas. Ecol Appl 16:1683–1695. doi:10.1890/1051-0761(2006)016[1683:OHOAEM]2.0.CO;2

    Article  Google Scholar 

  • Louzao M, Delord K, García D, Boué A, Weimerskirch H (2012) Protecting persistent dynamic oceanographic features: transboundary conservation efforts are needed for the critically endangered Balearic Shearwater. PLoS One 7(5):e35728. doi:10.1371/journal.pone.0035728

    Article  CAS  Google Scholar 

  • Luczak C, Beaugrand G, Jaffre M, Lenoir S (2011) Climate change impact on Balearic shearwater through a trophic cascade. Biol Lett 7:702–705. doi:10.1098/rsbl.2011.0225

    Article  CAS  Google Scholar 

  • Marques TA, Thomas L, Fancy SG, Buckland ST (2007) Improving estimates of bird density using multiple-covariate distance sampling. Auk 124:1229–1243. doi:10.1642/0004-8038(2007)124[1229:IEOBDU]2.0.CO;2

    Article  Google Scholar 

  • Mason E, Coombs S, Oliveira PB (2005) An overview of the literature concerning the oceanography of the eastern North Atlantic region. Relat. Cient. Téc. IPIMAR, Série digital, no 33, p 58. http://ipimar-iniap.ipimar.pt

  • Meirinho A, Barros N, Oliveira N, Catry P, Lecoq M, Paiva V, Geraldes P, Granadeiro JP, Ramírez I, Andrade J (2014) Atlas das Aves Marinhas de Portugal. Soc Port para o Estudo das Aves. Lisboa

  • Mouriño J, Arcos F, Salvadores R, Sandoval A, Vidal C (2003) Status of the Balearic shearwater (Puffinus mauretanicus) on the Galician coast (NW Iberian Peninsula). Sci Mar 62 (suppl 2):135–142

    Article  Google Scholar 

  • Nishizawa B, Matsuno K, Labunski EA, Kuletz KJ, Yamaguchi A, Watanuki Y (2015) Seasonal distribution of short-tailed shearwaters and their prey in the Bering and Chukchi Seas. Biogeosci Discuss 12:17721–17750. doi:10.5194/bgd-12-17721-2015

    Article  Google Scholar 

  • Noer H, Christensen TK, Clausager I, Petersen IK (2000) Effects on birds of an offshore wind park at Horns. Rev: Environmental impact assessment. NERI report 2000, p 65

  • Oppel S, Meirinho A, Ramírez I, Gardner B, O’Connell AF, Miller PI, Louzao M (2012) Comparison of five modelling techniques to predict the spatial distribution and abundance of seabirds. Biol Conserv 156:94–104. doi:10.1016/j.biocon.2011.11.013

    Article  Google Scholar 

  • Oro D, Aguilar JS, Igual JM, Louzao M (2004) Modelling demography and extinction risk in the endangered Balearic shearwater. Biol Conserv 116:93–102. doi:10.1016/S0006-3207(03)00180-0

    Article  Google Scholar 

  • Paiva VH, Werner A, Geraldes P, Ramirez I, Garthe S, Ramos JA (2013a) Overcoming difficult times: The behavioural resilience of a marine predator when facing environmental stochasticity. Mar Ecol Prog Ser 486:277–288. doi:10.3354/meps10332

    Article  Google Scholar 

  • Paiva VH, Geraldes P, Marques V, Rodríguez R, Garthe S, Ramos JA (2013b) Effects of environmental variability on different trophic levels of the North Atlantic food web. Mar Ecol Prog Ser 477:15–28. doi:10.3354/meps10180

    Article  Google Scholar 

  • Panigada S, Lauriano G, Burt L, Pierantonio N, Donovan G (2011) Monitoring winter and summer abundance of Cetaceans in the Pelagos sanctuary (Northwestern Mediterranean Sea) through aerial surveys. PLoS One 6(7):e22878. doi:10.1371/journal.pone.0022878

    Article  CAS  Google Scholar 

  • Pennycuick CJ (2002) Gust soaring as a basis for the flight of petrels and albatrosses (Procellariiformes). Avian Sci 2:1–12

    Google Scholar 

  • Perkins S, Sadoti G, Allison T, Jedrey E, Jones A (2005) Relative waterfowl abundance within Nantucket Sound, Massachusetts during the 2004–2005 winter season. Massachusetts Audubon Society Technical Report, Lincoln, MA, USA

  • 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

    Article  Google Scholar 

  • Peterson A, Papeş M, Eaton M (2007) Transferability and model evaluation in ecological niche modeling: a comparison of GARP and Maxent. Ecography 30:550–560. doi:10.1111/j.0906-7590.2007.05102.x

    Article  Google Scholar 

  • Petronilho JMS, Vingada JV, Ferreira M, Paulino NAC, Eira C, Costa R, Tenreiro PJQ (2004) Seabird census along the Figueira da Foz—Aveiro coastline (Portugal) during August/September 2002. Airo 14:94–100

    Google Scholar 

  • Phillips S (2006) A brief tutorial on Maxent. AT & T Research. http://www.cs.princeton.edu/~schapire/ma?xent/tutorial/tutorial.doc

  • Phillips S, Dudík M, Schapire R (2004) A maximum entropy approach to species distribution modeling. In: Brodley CE (ed) Proceedings of the 21st Century International Conference on Machine Learning. ACM Press, Banff, pp 655–662

    Google Scholar 

  • Phillips S, Anderson R, Schapire R (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. doi:10.1016/j.ecolmodel.2005.03.026

    Article  Google Scholar 

  • Poot M (2005) Large numbers of Balearic shearwater Puffinus mauretanicus along the Lisbon coast. Airo 15:43–50

    Google Scholar 

  • Porfirio LL, Harris RMB, Lefroy EC, Hugh S, Gould SF, Lee G, Bindoff NL, Mackey B (2014) Improving the Use of Species Distribution Models in Conservation Planning and Management under Climate Change. PLoS One 9(11): e113749. 10.1371/journal.pone.0113749

  • Ramírez I, Geraldes P, Merinho A, Amorim P, Paiva V (2008) Áreas Marinhas Importantes para as Aves em Portugal. Projecto LIFE04NAT/PT/000213. Sociedade Portuguesa Para o Estudo das Aves. Lisboa

  • Ridgway MS (2010) Line transect distance sampling in aerial surveys for double-crested cormorants in coastal regions of Lake Huron. J Great Lakes Res 36:403–410. doi:10.1016/j.jglr.2010.06.003

    Article  Google Scholar 

  • Rodda GH, Jarnevich CS, Reed RN (2011) Challenges in identifying sites climatically matched to the native ranges of animal invaders. PLoS One 6(2):e14670. doi:10.1371/journal.pone.0014670

    Article  CAS  Google Scholar 

  • Rodríguez A, García D, Rodríguez B, Cardona E, Parpal L, Pons P (2015) Artificial lights and seabirds: is light pollution a threat for the threatened Balearic petrels? J Ornithol 156:893–902. doi:10.1007/s10336-015-1232-3

    Article  Google Scholar 

  • Ronconi RA, Burger AE (2009) Estimating seabird densities from vessel transects: distance sampling and implications for strip transects. Aquat Biol 4:297–309. doi:10.3354/ab00112

    Article  Google Scholar 

  • Ruíz A, Martí R (2004) La Pardela Balear. SEO/BirdLife-Conselleria de Medi Ambient del Govem de les Illes Balears, Madrid

    Google Scholar 

  • Solanki HU, Mankodi PC, Nayak SR, Somvanshi VS (2005) Evaluation of remote-sensing-based potential fishing zones (PFZs) forecast methodology. Cont Shelf Res 25:2163–2173. doi:10.1016/j.csr.2005.08.025

    Article  Google Scholar 

  • Thaxter CB, Cook ASCP, Johnston A, Burton NHK (2011) Review of statistical techniques to model the at-sea distributions of breeding Sandwich Terns. British Trust for Ornithology, p 57. ISBN: 978-1-906204-89-1

  • Thomas L, Buckland ST, Rexstad EA, Laake JL, Strindberg S, Hedley SL, Bishop JRB, Marques TA, Burnham KP (2010) Distance software: design and analysis of distance sampling surveys for estimating population size. J Appl Ecol 47:5–14. doi:10.1111/j.1365-2664.2009.01737.x

    Article  Google Scholar 

  • Trenkel VM, Buckland ST, McLean C, Elson DA (1997) Evaluation of aerial line transect methodology for estimating red deer (Cervus elaphus) abundance in Scotland. J Environ Manage 50:39–50. doi:10.1006/jema.1996.0094

    Article  Google Scholar 

  • Warren DL, Glor RE, Turelli M (2010) ENMTools: a toolbox for comparative studies of environmental niche models. Ecography. doi:10.1111/j.1600-0587.2009.06142.x

    Google Scholar 

  • Winiarski KJ, Miller DL, Paton PWC, McWilliams SR (2013) A spatially explicit model of wintering common loons: Conservation implications. Mar Ecol Prog Ser 492:273–283. doi:10.3354/meps10492

    Article  Google Scholar 

  • Wisz MS, Hijmans RJ, Li J, Peterson AT, Graham CH, Guisan A, NCEAS Predicting Species Distributions Working Group (2008) Effects of sample size on the performance of species distribution models. Divers Distrib 14:763–773. doi:10.1111/j.1472-4642.2008.00482.x

    Article  Google Scholar 

  • Wynn RB, Yésou P (2007) The changing status of Balearic Shearwater in northwest European waters. Br Birds 100:392–406

    Google Scholar 

  • Wynn RB, Josey SA, Martin A, Johns DG, Yésou P (2007) Climate-driven range expansion of a critically endangered top predator in northeast Atlantic waters. Biol Lett 3:529–532. doi:10.1098/rsbl.2007.0162

    Article  Google Scholar 

  • Yésou P (2003) Recent changes in the summer distribution of the Balearic shearwater Puffinus mauretanicus off western France. Sci Mar 67 (suppl 2):143–148

    Article  Google Scholar 

Download references

Acknowledgements

This work was partly funded by the Portuguese Wildlife Society and projects SafeSea EEA-Grants, FAME (Proj. 2009-1/089) and European Commission’s Life Programme (MarPro NAT/PT/00038). This study was also partly supported by the Portuguese Foundation for Science and Technology (FCT) with Grants SFRH/ BD/30240/2006 to M. Ferreira and SFRH/BD/32841/2006 to P. C. Rodrigues. C. Eira is supported by FCT through CESAM UID/AMB/50017/2013 co-funded by FCT/MEC and FEDER, within PT2020 and Compete 2020 and S. Monteiro is financed by a Grant (BPD/0043/AMB/50017) from UID/AMB/50017/2013. This work was also partially supported by the strategic programme UID/BIA/04050/2013 (POCI-01-0145-FEDER-007569) funded by FCT and by ERDF (COMPETE2020). The authors thank observers and airplane pilots who contributed to this work.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hélder Araújo.

Ethics declarations

Conflict of interest

All authors declare they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Responsible Editor: V. Paiva.

Reviewed by undisclosed experts.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 3536 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Araújo, H., Bastos-Santos, J., Rodrigues, P.C. et al. The importance of Portuguese Continental Shelf Waters to Balearic Shearwaters revealed by aerial census. Mar Biol 164, 55 (2017). https://doi.org/10.1007/s00227-017-3089-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-017-3089-x

Keywords

Navigation