Abstract
Thousands of marine animals are injured and killed each year across Europe. Wildlife rehabilitation centres play an important role to rehabilitate sick and injured animals and return them to the wild. This study aims to assess seabird rehabilitation outcomes and causes of mortality of stranded seabirds in the central Portuguese coast. During a 7-year period (2010–2016) a total of 2042 admissions were registered, including 1135 live and 907 dead seabirds. The main causes for live admissions were trauma (30%) and toxicity (29.5%) and the main cause of all admissions (dead and alive) was entanglement/bycatch representing 42.5% of all seabirds. Large gulls, auks, gannets, and shearwaters and petrels were the most admitted seabird groups. A total of 445 seabirds (39%) were released to the wild following rehabilitation, 346 (31%) died during the rehabilitation process and 344 (30%) were considered untreatable after diagnosis and were euthanised. Considering the rehabilitation success rate and the high number of individuals admitted due to causes associated with human activities (entanglement/bycatch, trauma), marine animal rehabilitation centres and stranding networks are important to seabird conservation. These data also contribute to monitor the impacts of human activities on seabird populations outside their breeding areas.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10344-021-01483-5/MediaObjects/10344_2021_1483_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10344-021-01483-5/MediaObjects/10344_2021_1483_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10344-021-01483-5/MediaObjects/10344_2021_1483_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10344-021-01483-5/MediaObjects/10344_2021_1483_Fig4_HTML.png)
Similar content being viewed by others
Data availability
The datasets used and analysed during the current study are available from the corresponding author on reasonable request.
References
Almpanidou V, Tsapalou V, Tsavdaridou AI, Mazris A (2020) The dark side of raptors’ distribution ranges under climate change. Landscape Ecol 35:1435–1443
Anon (2009) BWRC-Wildlife Casualty Recording Scheme. British Wildlife Rehabilitation Council, UK http://wildlife1.widllifeinformation.org/S/00Ref/miscellaneouscontents/BWRC-CasualtyRecordingScheme/Titlepage.htm
Artyukhin YB, Burkanov VN (2000) Incidental mortality of seabirds in the drift net salmon fishery by Japanese vessels in the Russian Exclusive Economic Zone, 1993–97. In: Kondratyev AY, Litvinenko NM, Kaiser GW (eds) Seabirds of the Russian Far East. Canadian Wildlife Service, Ottawa, ON, pp 105–115
Balmori A (2019) Endangered bird mortality by gunshots: still a current problem. Biodivers Conserv 28:2555–2564
Barnett J, Westcott S (2001) Distribution, demographics and survivorship of grey seal pups (Halichoerus grypus) rehabilitated in southwest England. Mammalia 65(3):349–361
Beja (1989) Beja PR (1989) A note on the diet of Razorbills Alca torda wintering off Portugal. Seabird 12:11–13
Benjamins S, Kulka DW, Lawson J (2008) Incidental catch of seabirds in Newfoundland and Labrador gillnet fisheries, 2001–2003. Endang Species Res 5:149–160
Brothers N, Duckworth AR, Safina C, Gilman EL (2010) Seabird bycatch in pelagic longline fisheries is grossly underestimated when using only haul data. PLoS ONE 5(8):e12491. https://doi.org/10.1371/journal.pone.0012491
Camphuysen CJ (2013) Monitoring and assessment of the proportion of oiled Common Guillemots from beached bird surveys in The Netherlands: update winter 2012/13. Report commissioned by the Ministry of Infrastructure and the Environment (I&M), RWS Water, Traffic and Living Environment (RWS-WVL) and DG Mobility and Transport (DGB). Royal Netherlands Institute for Sea Research, Texel.
Catry P, Costa H, Elias G, Matias R (2010) Aves de Portugal. Ornitologia do território continental. Assírio & Alvim, Lisboa
Costa RA, Pereira AT, Costa E, Henriques AC, Miodonski J, Ferreira M, Vingada JV, Eira C (2019) Razorbill Alca torda mortality in the Portuguese west coast. Eur J Wildlife Res 65:3
Costa RA, Sá S, Pereira AT, Ângelo AR, Vaqueiro J, Ferreira M, Eira C (2020) Prevalence of entanglements of seabirds in marine debris in the central Portuguese coast. Marine Pollution Bulletin 161:111746
Dau BK, Gilardi KVK, Gulland FM, Higgins A, Holcomb JB, St. Leger J, Ziccardi MH (2009) Fishing gear–related injury in California marine wildlife. J Wildl Dis 45(2):355–362
Davoren GK (2007) Effects of gill-net fishing on marine birds in a biological hotspot in the Northwest Atlantic. Conserv Biol 21:1032–1045
Deem SL, Terrell SP, Forrester DJ (1998) A retrospective study of morbidity and mortality of raptors in Florida: 1988–1994. J Zoo Wildl Med 29(2):160–164
del Hoyo J, Elliot A, Sargatal J (1992) Handbook of the birds of the world, vol 1: ostrich to ducks. Lynx Edicions, Barcelona, Spain
Du Toit J (1999) A hel** hand. Africa Birds and Birding 4(3):60–63
EURING (1994) El anillamiento de aves: herramienta científica y de gestión ambiental. Dirección General de Conservación de la Naturaleza-SEO/BirdLife, Madrid
Garcês A, Pires I, Pacheco FAL, Fernandes LFS, Soeiro V, Lóio S, Prada J, Cortes R, Queiroga FL (2019a) Preservation of wild bird species in northern Portugal – effects of anthropogenic pressures in wild bird populations (2008–2017). Sci Total Environ 650:2996–3006
Garcês A, Pires I, Pacheco F, Fernandes LS, Soeiro V, Lóio S, Prada J, Cortes R, Queiroga F (2019b) Natural and anthropogenic causes of mortality in wild birds in a wildlife rehabilitation centre in Northern Portugal: a ten-year study. Bird Study 66(4):484–493
Garcês A, Queiroga F, Prada J, Pires I (2020) A review of the mortality of wild fauna in Europe in the last century: the consequences of human activity. Journal of Wildlife and Biodiversity 4(2):34–55
Garthe S, Scherp B (2003) Utilization of discards and offal from commercial fisheries by seabirds in the Baltic Sea. Ices J Mar Sci 60(5):980–989
Glaser LC (1999) Organophosphorus and carbamate pesticides. In: Friend M, Franson JC (eds) Field manual of wildlife diseases: general field procedures and diseases of birds. U.S. Geological Survey, Washington DC, pp 287–293
Good TP, June JA, Etnier MA, Broadhurst G (2009) Ghosts of the Salish Sea: threats to marine birds in Puget Sound and the Northwest Straits from derelict fishing gear. Mar Ornithol 37:67–76
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. https://doi.org/10.1371/journal.pone.0033753
Hamel NJ, Burger AE, Charleton K, Davidson P, Lee S, Bertram DF, Parrish JK (2009) Bycatch and beached birds: assessing mortality impacts in coastal net fisheries using marine bird strandings. Mar Ornithol 37:41–60
Harden J (2002) An overview of anthropogenic causes of avian mortality. J Wildlife Rehabil 25:4–11
Harden J, Dickerman RW, Elliston EP (2006) Collection, value, and use of wildlife rehabilitation data. J Wildlife Rehabil 28(1):10–28
Humple D, Abraham C, Ramos A, Dopico M, Fernández-Boán M, García L, Bao R, Heubeck M, Camphuysen CJ (2007) Age and sex structure of auk (Alcidae) mortality during the Prestige oil spill in Galicia, NW Spain, November 2002–April 2003. In: Conference Proceedings of the Ninth International Effects of Oil on Wildlife Conference, Monterey, California
IBM Corp. Released (2016) IBM SPSS Statistics for Macintosh, version 24.0. IBM Corp, Armonk, NY
INE (2017) Estatísticas da Pesca 2017. Instituto Nacional de Estatística, I.P. Lisboa, Portugal.
Kalpakis S, Mazaris AD, Mamakis Y, Poulopoulos Y (2009) A retrospective study of mortality and morbidity factors for common buzzards Buteo buteo and long-legged buzzards Buteo rufinus in Greece: 1996–2005. Bird Conserv Int 19(1):15–21
Kwon Y-K, Wee S-H, Kim J-H (2004) Pesticide poisoning in wild birds in Korea from 1998 to 2002. Short communications. J Wildl Dis 40(4):737–740
Lehikoinen A, Lindén A, Karlsson M, Andersson A, Crewe TL, Dunn EH, Gregory G, Karlsson L, Kristiansen V, Mackenzie S, Newman S, Røer JE, Sharpe C, Sokolov LV, Steinholtz A, Stervander M, Tirri I, Tjørnløv RS (2019) Phenology of the avian spring migratory passage in Europe and North America: asymmetric advancement in time and increase in duration. Ecol Indic 10:985–991
Lewis L, Schweitzer SH (2000) Lead poisoning in a Northern bobwhite in Georgia. J Wildl Dis 36:180–183
Lovvorm JR (2007) Modeling oil spill impacts on seabirds, with special reference to Cassin’s auklets. In: Conference Proceedings of the Ninth International Effects of Oil on Wildlife Conference, Monterey, California
Martínez-Haro M, Vinuela J, Mateo R (2007) Exposure of birds to cholinesterase-inhibiting pesticides following a forest application for tick control. Environ Toxicol Pharmacol 23(3):347–349
Mazaris A, Mamakis Y, Kalpakis S, Poulopoulos Y, Matsinos Y (2008) Evaluating potential threats to birds in Greece: an analysis of a 10-year data set from a rehabilitation centre. Fauna and Flora International, Oryx 42(3):408–414
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. Sociedade Portuguesa para o Estudo das Aves, Lisboa
Molina-López RA, Casal J, Darwich L (2013) Final disposition and quality auditing of the rehabilitation process in wild raptors admitted to a wildlife rehabilitation centre in Catalonia, Spain, during a twelve year period (1995–2007). PLoS ONE 8(4):e60242. https://doi.org/10.1371/journal.pone.0060242
Molina-López RA, Mañosa S, Torres-Riera A, Pomarol M, Darwich L (2017) Morbidity, outcomes and cost–benefit analysis of wildlife rehabilitation in Catalonia (Spain). PLoS ONE 12(7):e0181331. https://doi.org/10.1371/journal.pone.0181331
Montesdeoca N, Calabuig P, Corbera JA, Orós J (2017) A long-term retrospective study on rehabilitation of seabirds in Gran Canaria Island, Spain (2003–2013). PLoS ONE 12(5):e0177366
Moore JE, Wallace BP, Lewison RL, Zydelis R, Cox TM, Crowder LB (2009) A review of marine mammal, sea turtle and seabird bycatch in USA fisheries. Mar Policy 33(3):435–451
Moore KM, Simeone CA, Brownell L Jr (2018) Strandings. In: Würsig B, Thewissen JGM, Kovacs KM (eds) Encyclopedia of marine mammals (third edition). Academic Press, pp 945–951
Nadal J, Ponz C, Margalida A, Pennisi L (2020) Ecological markers to monitor migratory bird populations: integrating citizen science and transboundary management for conservation purposes. J Environ Manage 255:109875
Nelson B (2002) The Atlantic gannet, 2nd edn. Fenix Books, Norfolk
Olsen KM, Larsson H (2004) Gulls of North America, Europe, and Asia, 2nd edn. Princeton University Press
Österblom H, Fransson T, Olsson O (2002) Bycatches of Common Guillemot (Uria aalge) in the Baltic Sea gillnet fishery. Biol Conserv 105:309–319
Pellissier V, Schmucki R, Pe’er G, Aunins A, Brereton TM, Brotons L, Carnicer J, Chodkiewicz T, Chylarecki P, del Moral JC, Escandell V, Evans D, Foppen R, Harpke A, Heliola J, Herrando S, Kuussaari M, Kuhn E, Lehikoinen A, Lindstrom A, Moshøj CM, Musche M, Noble D, Oliver TH, Reif J, Richard D, Roy DB, Schweiger O, Settele J, Stefanescu C, Teufelbauer N, Touroult J, Trautmann S, van Strien AJ, van Swaay CAM, van Turnhout C, Vermouzek Z, Vorısek P, Jiguet F, Julliard R (2019) Effects of Natura 2000 on nontarget bird and butterfly species based on citizen science data. Conserv Biol 34(3):666–676
Pikula J, Hajkova P, Bandouchova H, Bednarova I, Adam V, Bemklova M, Kral J, Ondracek K, Osickova J, Pohanka M, Sedlackova J, Skochova H, Sobotka J, Treml F, Kizek R (2013) Lead toxicosis of captive vultures: case description and responses to chelation therapy. BMC Vet Res 9(11):1–10
Reeve NJ, Huijser MP (1999) Mortality factors affecting wild hedgehogs: a study of records from wildlife rescue centers. Lutra 42:6–24
Riotte-Lambert L, Weimerskirch H (2013) Do naive juvenile seabirds forage differently from adults? Proc. R. Soc. B 280:20131434
Rock P (2005) Urban gulls: problems and solutions. British birds 98:338–355
Rodríguez B, Rodríguez A, Siverio F, Siverio M (2010) Causes of raptor admissions to a wildlife rehabilitation center in Tenerife (Canary Islands). J Raptor Res 44(1):30–39
Seamans TW, Belant JL (1999) Comparison of DRC-1339 and alpha-chloralose to reduce herring gull populations. Wildl Soc Bull 27(3):729–733
Shumway SE, Allen SM, Dee Boersma P (2003) Marine birds and harmful algal blooms: sporadic victims or under-reported events? Harmful Algae 2:1–17
Soares SPV (2014) Paretic syndrome in gulls (Laridae) in the south of Portugal. M.Sc. thesis, Faculdade de Medicina Veterinária, Lisbon University.
Steele CM, Brown RN, Botzler RG (2005) Prevalences of zoonotic bacteria among seabirds in rehabilitation centers along the Pacific Coast of California and Washington, USA. J Wildl Dis 41(4):735–744
Stone WB, Overmann SR, Okoniewski JC (1984) Intentional poisoning of birds with parathion. The Condor 86(3):333–336
Thompson RP (2013) Factors influencing the admission of urban nesting Herring Gulls Larus argentatus into a rehabilitation centre and post release survival in comparison with wild counterparts. University of Sussex DPhil thesis.
Troisi G, Barton S, Bexton S (2016) Impacts of oil spills on seabirds: unsustainable impacts of non-renewable energy. International Journal of Hydrogen Energy 41(37):16549–16555
Wells ML, Trainer VL, Smayda TJ, Karlson BSO, Trick CG, Kudela RM, Ishikawa A, Bernard S, Wulff A, Anderson DM, Cochlan WP (2015) Harmful algal blooms and climate change: learning from the past and present to forecast the future. Harmful Algae 49:68–93
Whitney H (2004) Wildlife diseases fact sheet: Pesticide poisoning of seagulls. Government of Newfoundland and Labrador – Department of Natural Resources, AP051
Willette M, Ponder J, McRuer DL, Clark EE Jr (2013) Wildlife health monitoring systems in North America: from sentinel species to public policy. In: Aguirre A (ed) Conservation Medicine: Applied Cases of Ecological Health
Wimberger K, Downs CT (2010) Annual intake trends of a large urban animal rehabilitation centre in South Africa: a case study. Anim Welfare 19:501–513
Zydelis R, Small C, French G (2013) The incidental catch of seabirds in gillnet fisheries: a global review. Biol Conserv 162:76–88
Acknowledgements
The authors wish to thank everyone who reported and collected seabirds, including the Maritime Authority and the Republican National Guard (GNR-SEPNA) and all the staff and volunteers of the stranding network and rehabilitation centres CRAM-Q and CRAM-Ecomare.
Funding
This study was partly supported by the Portuguese Foundation for Science and Technology (FCT) with Grants attributed to R.A.C. (SFRH/BPD/99394/2013), to S.S. (PD/BD/127920/2016), to A.T.P. (SFRH/BD/122890/2016) and to M.F. (SFRH/BD/30240/2006). R.A.C. is funded by national funds (OE), through FCT—Fundação para a Ciência e a Tecnologia, I.P., in the scope of the framework contract foreseen in the numbers 4, 5 and 6 of article 23, of the Decree-Law 57/2016, of August 29, changed by Law 57/2017, of July 19. C.E. is supported at CESAM (UID/AMB/50017) by FCT/MCTES, through national funds and co-funding by FEDER, within the PT2020 Partnership Agreement and Compete 2020 (POCI-01-0145-FEDER-007638). Thanks are due for the financial support to CESAM (UIDP/50017/2020 + UIDB/50017/2020) through national funds.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethics approval
This study was conducted in accordance with all applicable laws and rules dictated by the Portuguese Government and all licenses granted by Institute for Nature and Forest Conservation (ICNF). Samples from stranded birds are archived in the Marine Animal Tissue bank (13PT0124/S) recognised by the ICNF with CITES permit code PT009 to maintain samples.
Consent for publication
All authors read and approved the final manuscript.
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
J. V. Vingada Deceased 19 March 2019
Rights and permissions
About this article
Cite this article
Costa, R.A., Sá, S., Pereira, A.T. et al. Threats to seabirds in Portugal: integrating data from a rehabilitation centre and stranding network. Eur J Wildl Res 67, 41 (2021). https://doi.org/10.1007/s10344-021-01483-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10344-021-01483-5