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An overview of seabirds in the Santos Basin, Brazil: species, threats, and current trends in studies

Abstract

The Santos Basin in eastern Brazil is adjacent to the largest human populations in the southwestern Atlantic Ocean, with several potential threats to marine vertebrates. In this study, we provided a systematic bibliographic review and integrated unpublished primary datasets to provide an overview on species, research topics and gaps, and threats to seabirds in the Santos Basin. Bibliographical sources were used for species recorded within the limits of the basin, while species census data were obtained through research and monitoring projects. We analyzed 156 studies from 1914 to 2021. An increase in the number of publications was observed from the 2000s onward (> 80%), with the state of Santa Catarina showing the highest number of publications (56%) on seabirds. Notes and Records (27%), Population and Community Structure (22%), and Fishing (11%) were the main subjects studied. Among the 76 seabird species reported in the Santos Basin (~2/3 of the species reported in Brazil), Procellariiformes was the most prevalent order (51%), including 14 species listed as threatened, either globally or nationally. Resident (28%) and long-distance migratory species, such as visitors from the Southern (39%) and Northern (17%) Hemispheres and Europe (12%), were widely recorded in the region, as well as vagrant species. The inclusion of different data sources allowed broadening the geographic cover used by species to consider both coastal (predominating in previous studies) and offshore areas. The association of seabird distribution with oceanographic and meteorological features should be addressed in future studies, as should studies on the impact of fishing and pollution on a range of common species.

Descriptors:
At-sea distribution; Biodiversity; Ornithological records; Research priorities; Southeastern Brazil

INTRODUCTION

Seabirds are generally defined as species that depend on marine resources and that breed either on islands or coastal areas (Schreiber and Burger, 2001SCHREIBER, E. A. & BURGER J. 2001. Biology of Marine Birds. London: CRC Press.). However, this somewhat restrictive definition excludes most coastal birds, which are included in the definition proposed by Vooren and Brusque (1999)VOOREN, C. M. & BRUSQUE, L. 1999. Diagnóstico sobre as aves do ambiente costeiro do Brasil [online]. In: Avaliação e Ações Prioritárias para Conservação da Biodiversidade da Zona Costeira e Marinha Pronabio. Rio Grande: Fundação Universidade Federal de Rio Grande, 125 pp. Available at: https://www.yumpu.com/pt/document/view/12874470/as-aves-do-ambiente-costeiro-do-brasil-viva-marajo. [Accessed: 2021 Oct 07].
https://www.yumpu.com/pt/document/view/1...
, as birds that either feed on the beach or carry out kleptoparasitism on other birds, in addition to those that are strictly marine. As such, seabird species considered as marine may vary according to the criteria adopted by the author. According to Vooren and Brusque (1999)VOOREN, C. M. & BRUSQUE, L. 1999. Diagnóstico sobre as aves do ambiente costeiro do Brasil [online]. In: Avaliação e Ações Prioritárias para Conservação da Biodiversidade da Zona Costeira e Marinha Pronabio. Rio Grande: Fundação Universidade Federal de Rio Grande, 125 pp. Available at: https://www.yumpu.com/pt/document/view/12874470/as-aves-do-ambiente-costeiro-do-brasil-viva-marajo. [Accessed: 2021 Oct 07].
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, there are at least 148 species in Brazil, distributed between coastal and pelagic birds, although this includes many coastal birds excluded from most definitions. In a recent study, Nunes et al. (2023)NUNES, G. T., EFE, M. A., SERAFINI, P. P. & BUGONI, L. 2023. Aves marinhas no Brasil: ações para a conservação. Oecologia Australis. [in press] mention 100 seabird species occurring in Brazil, based on the recent Brazilian bird species list (Pacheco et al., 2021PACHECO, J. F., SILVEIRA, L. F., ALEIXO, A., AGNE, C. E., BENCKE, G. A., BRAVO, G. A., BRITO, G. R. R., COHN-HAFT, M., MAURÍCIO, G. N., NAKA, L. N., OLMOS, F., POSSO, S., LEES, A. C., FIGUEIREDO, L. F. A., CARRANO, E., GUEDES, R. C., CESARI, E., FRANZ, I., SCHUNCK, F. & PIACENTINI, V. Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee – second edition. Ornithology Research, 29(2), 94-105, DOI: https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
). Among the species occurring in Brazil, many breed on coastal islands (e.g. Campos et al., 2004CAMPOS, F. P., PALUDO, D., FARIA, P. J. & MARTUSCELLI, P. 2004. Aves insulares marinhas, residentes e migratórias, do litoral do estado de São Paulo. In: BRANCO, J. O. (ed.). Aves Marinhas Insulares Brasileiras: Bioecologia e Conservação. Itajaí: Editora da UNIVALI, pp. 57-82.) and oceanic islands (Mancini et al., 2016MANCINI, P. L., SERAFINI, P. P. & BUGONI, L. 2016. Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Revista Brasileira de Ornitologia, 24(2), 94-115, DOI: https://doi.org/10.1007/BF03544338
https://doi.org/10.1007/BF03544338...
), in addition to a number of migrants from both hemispheres (Somenzari et al., 2018SOMENZARI, M., AMARAL, P. P., CUETO, V. R., GUARALDO, A. C., JAHN, A. E., LIMA, D. M., LIMA, P. C., LUGARINI, C., MACHADO, C. G., MARTINEZ, J., NASCIMENTO, J. L. X., PACHECO, J. F., PALUDO, D., PRESTES, N. P. , SERAFINI, P. P. , SILVEIRA, L. F., SOUSA, A. E. B. A., SOUSA, N. A., SOUZA, M. A., TELINO-JÚNIOR, W. R. & WHITNEY, B. M. 2018. An overview of migratory birds in Brazil. Papéis Avulsos de Zoologia, 58, e20185803, DOI: https://doi.org/10.11606/1807-0205/2018.58.03
https://doi.org/10.11606/1807-0205/2018....
), and some are vagrants, i.e., of occasional occurrence outside their regular distribution area (Dias et al., 2012DIAS, R. A., AGNE, C. E., BARCELOS-SILVEIRA, A. & BUGONI, L. 2012. New records and a review of the distribution of the Arctic Tern Sterna paradisaea Pontoppidan, 1763 (Aves: Sternidae) in Brazil. Check List, 8(3), 563-567, DOI: https://doi.org/10.15560/8.3.563
https://doi.org/10.15560/8.3.563...
). The Santos Basin is a vast area located across the south and southeast regions of Brazil, in a subtropical region close to a tropical area such that it receives migratory species from various latitudes and species that breed in the several adjacent coastal islands (Campos et al., 2004CAMPOS, F. P., PALUDO, D., FARIA, P. J. & MARTUSCELLI, P. 2004. Aves insulares marinhas, residentes e migratórias, do litoral do estado de São Paulo. In: BRANCO, J. O. (ed.). Aves Marinhas Insulares Brasileiras: Bioecologia e Conservação. Itajaí: Editora da UNIVALI, pp. 57-82.). This important area for resident and migratory seabirds is under a range of anthropogenic threats including contamination of the marine environment, fishing activities, and various impacts associated to coastal occupation.

Furthermore, seabirds are excellent indicators of the quality of the ocean (Furness and Camphuysen, 1997FURNESS, R. W. & CAMPHUYSEN, K. 1997. Seabirds as monitors of the marine environment. ICES Journal of Marine Science, 54(4), 726-737, DOI: https://doi.org/10.1006/jmsc.1997.0243
https://doi.org/10.1006/jmsc.1997.0243...
; Burger and Gochfeld, 2004BURGER, J. & GOCHFELD, M. 2004. Marine birds as sentinels of environmental pollution. EcoHealth, 1(3), 263-274, DOI: https://doi.org/10.1007/s10393-004-0096-4
https://doi.org/10.1007/s10393-004-0096-...
) because they respond quickly to changes in the environment, making them key components in the marine ecosystem. They are top predators of the trophic chain, have long life spans, inhabit vast home ranges, and migrate long distances, in addition to occurring in areas ranging from coastal to pelagic waters, from tropical to polar regions (Schreiber and Burger, 2001SCHREIBER, E. A. & BURGER J. 2001. Biology of Marine Birds. London: CRC Press.; Spear et al., 2001SPEAR, L. B., BALLANCE, L. T. & AINLEY, D. G. 2001. Response of seabirds to thermal boundaries in the tropical Pacific: the thermocline versus the Equatorial Front. Marine Ecology Progress Series, 219, 275-289, DOI: https://doi.org/10.3354/meps219275
https://doi.org/10.3354/meps219275...
; González-Solís et al., 2007GONZÁLEZ-SOLÍS, J., CROXALL, J. P., ORO, D. & RUIZ, X. 2007. Trans-equatorial migration and mixing in the wintering areas of a pelagic seabird. Frontiers in the Ecology and Environment, 5(6), 297-301, DOI: https://doi.org/10.1890/1540-9295(2007)5[297:TMAMIT]2.0.CO;2
https://doi.org/10.1890/1540-9295(2007)5...
). The use of seabirds as environmental indicators has some advantages, such as easy sampling during breeding periods when birds concentrate in colonies, and fidelity to breeding area (Schreiber and Burger, 2001SCHREIBER, E. A. & BURGER J. 2001. Biology of Marine Birds. London: CRC Press.; Petry et al., 2018PETRY, M. V., VALLS, F. C. L., PETERSEN, E. S., FINGER, J. V. & KRÜGER, L. 2018. Population trends of seabirds at Stinker Point, Elephant Island, Maritime Antarctica. Antarctic Science, 30(4), 220-226, DOI: https://doi.org/10.1017/S0954102018000135
https://doi.org/10.1017/S095410201800013...
). During non-breeding periods, birds may use different habitats, allowing them to assess different levels and compartments of the ecosystem throughout the year (e.g. Robuck et al., 2022ROBUCK, A. R., HUDAK, C. A., AGVENT, L., EMERY, G., RYAN, P. G., PEROLD, V., POWERS, K. D., PEDERSEN, J., THOMPSON, M. A., SUCA, J. J., MOORE, M. J., HARMS, C. A., BUGONI, L., SHIELD, G., GLASS, T., WILEY, D. N. & LOHMANN R. 2022. Birds of a feather eat plastic together: high levels of plastic ingestion in Great Shearwater adults and juveniles across their annual migratory cycle. Frontiers in Marine Science, 8, 719721, DOI: https://doi.org/10.3389/fmars.2021.719721
https://doi.org/10.3389/fmars.2021.71972...
).

Along the Atlantic coast of South America, cold currents from polar regions, such as the Malvinas Current, reach the southern coast of Brazil, providing great diversity of organisms and a high biomass of food resources for these top predators (Veit and Braun, 1984VEIT, R. R. & BRAUN, R. M. 1984. Hydrographic fronts and marine birds distribution in Antarctic and SubAntarctic waters. Antarctic Journal of the United States, 19(5), 165-167.; Orgeira, 1995ORGEIRA, T. J. L. 1995. Seabird observations of the Argentina Atlantic shore between Tierra del Fuego and Buenos Aires. Bolletino-Museo Regionale di Scienze Naturali, 13(1), 105-115.; Montalti and Orgeira, 1998MONTALTI, D. & ORGEIRA, J. L. 1998. Distribución de aves marinas en la costa patagónica Argentina. Ornitología Neotropical, 9(2), 193-199.). In turn, the Brazil Current, moving from the north, reaches southern Brazil with temperature and salinity above 20 °C and 36 PSU, respectively (Silveira et al., 2000SILVEIRA, I. C. A., SCHMIDT, A. C. K., CAMPOS, E. J. D., GODOI, S. S. D. & IKEDA, Y. 2000. A corrente do Brasil ao largo da costa leste brasileira. Brazilian Journal of Oceanography, 48(2), 171-183, DOI: https://doi.org/10.1590/S1413-77392000000200008
https://doi.org/10.1590/S1413-7739200000...
). Therefore, migratory birds from the Southern and Northern Hemispheres are often observed either during their movement periods or while using the coast of Brazil as non-breeding areas (Vooren and Fernandes, 1989VOOREN, C. M. & FERNANDES, A. C. 1989. Guia de Albatrozes e Petréis do Sul do Brasil. Porto Alegre: Editora Sagra.; Ramirez et al., 2013RAMIREZ, I., PAIVA, V. H., MENEZES, D., SILVA, I., PHILLIPS, R. A., RAMOS, J. A. & GARTHE, S. 2013. Year-round distribution and habitat preferences of the Bugio Petrel. Marine Ecology Progress Series, 476, 269-284, DOI: https://doi.org/10.3354/meps10083
https://doi.org/10.3354/meps10083...
; Ramos et al., 2017RAMOS, R., CARLILE, N., MADEIROS, J., RAMIREZ, I., PAIVA, V. H., DINIS, H. A., ZINO, F., BISCOITO, M., LEAL, G. R., BUGONI, L., JODICE, P. G. R., RYAN, P. G. & GONZÁLEZ-SOLÍS, J. 2017. It is the time for oceanic seabirds: tracking year‐round distribution of gadfly petrels across the Atlantic Ocean. Diversity and Distributions, 23(7), 794-805, DOI: https://doi.org/10.1111/ddi.12569
https://doi.org/10.1111/ddi.12569...
). At this stage of their life cycle, seabirds are under anthropic threats from activities that occur in the region (Petry and Fonseca, 2002PETRY, M. V. & FONSECA V. S. S. 2002. Effects of human activities in the marine environment on seabirds along the coast of Rio Grande do Sul, Brazil. Ornitología Neotropical, 13(2), 137-142.; Valls et al., 2015VALLS, F. C. L., SANTOS, C. R., BASLER, A. B. & PETRY, M. V. 2015. New record on the occurrence of Northern Giant Petrel (Macronectes halli) and analysis of stomach contents in southern Brazil. Pan-American Journal of Aquatic Sciences, 10(4), 309-314.), which can result in substantial environmental changes and lead to ecological imbalance (Baum and Worm, 2009BAUM, J. K. & WORM, B. 2009. Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology, 78(4), 699-714, DOI: https://doi.org/10.1111/j.1365-2656.2009.01531.x
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). An increasing number of studies have reported problems related to climate change, the exploitation of natural resources, and the release of pollutants into the ocean (e.g. Doney et al., 2012DONEY, S. C., RUCKELSHAUS, M., DUFFY, J. M., BARRY, J. P., CHAN, F., ENGLISH, C. A. GALINDO, H. M, GREBMEIR, J. M., HOLOWED, A. B., KNOWLTON, N., POLOVINA, J., RABALAIS, N. N., SYDEMAN, J. L. & TALLEY, L. D. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4, 11-37, DOI: https://doi.org/10.1146/annurev-marine-041911-111611
https://doi.org/10.1146/annurev-marine-0...
; Kühn et al., 2020KÜHN, S. & VAN FRANEKER, J. A. 2020. Quantitative overview of marine debris ingested by marine megafauna. Marine Pollution Bulletin, 151, 110858, DOI: https://doi.org/10.1016/j.marpolbul.2019.110858
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; Hatje et al., 2021HATJE, V., ANDRADE, R. L., OLIVEIRA, C. C. D., POLEJACK, A. & GXABA, T. 2021. Pollutants in the South Atlantic Ocean: sources, knowledge gaps and perspectives for the decade of Ocean Science. Frontiers in Marine Science, 8, 644569, DOI: https://doi.org/10.3389/fmars.2021.644569
https://doi.org/10.3389/fmars.2021.64456...
; Belhabib and Le Billon, 2022BELHABIB, D. & LE BILLON, P. 2022. Fish crimes in the global oceans. Science Advances, 8(12), eabj1927, DOI: https://doi.org/10.1126/sciadv.abj1927
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; Nunes et al., 2022NUNES, G. T., EFE, M. A., BARRETO, C. T., GAIOTTO, J. V., SILVA, A. B., VILELA, F., ROY, A., BERTRAND, S., COSTA, P. G., BIANCHINI, A. & BUGONI, L. 2022. Ecological trap for seabirds due to the contamination caused by the Fundão Dam collapse, Brazil. Science of the Total Environment, 807(Pt 2), 151486, DOI: https://doi.org/10.1016/j.scitotenv.2021.151486
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), reinforcing the importance of detecting and monitoring their potential effects on marine ecosystems.

Anthropic activities such as pollution and longline, gillnet, and trawl fishing are high-impact threats to birds, causing mortality of different species (Wiese and Ryan, 2003WIESE, F. K. & RYAN, P. C. 2003. The extent of chronic marine oil pollution in southeastern Newfoundland waters assessed through beached bird surveys 1984-1999. Marine Pollution Bulletin, 46(9), 1090-1101, DOI: https://doi.org/10.1016/S0025-326X(03)00250-9
https://doi.org/10.1016/S0025-326X(03)00...
; Branco et al., 2014BRANCO, J. O., FRACASSO, H. A. A., PÉREZ, J. A. A. & RODRIGUES FILHO, J. L. 2014. An assessment of oceanic seabird abundance and distribution off the southern Brazilian coast using observations obtained during deep-water fishing operations. Brazilian Journal of Biology, 74(3 Suppl 1), S003-S015, DOI: https://doi.org/10.1590/1519-6984.13612
https://doi.org/10.1590/1519-6984.13612...
; Dias et al., 2019DIAS, M. P., MARTIN, R., PEARMAIN, E. J., BURFIELD, I. J., SMALL, C., PHILLIPS, R. A. & CROXALL, J. P. 2019. Threats to seabirds: a global assessment. Biological Conservation, 237, 525-537, DOI: https://doi.org/10.1016/j.biocon.2019.06.033
https://doi.org/10.1016/j.biocon.2019.06...
; Nunes et al., 2022NUNES, G. T., EFE, M. A., BARRETO, C. T., GAIOTTO, J. V., SILVA, A. B., VILELA, F., ROY, A., BERTRAND, S., COSTA, P. G., BIANCHINI, A. & BUGONI, L. 2022. Ecological trap for seabirds due to the contamination caused by the Fundão Dam collapse, Brazil. Science of the Total Environment, 807(Pt 2), 151486, DOI: https://doi.org/10.1016/j.scitotenv.2021.151486
https://doi.org/10.1016/j.scitotenv.2021...
). Among others, metals, persistent organic pollutants, solid waste, and oil spills can affect seabirds, with effects ranging from lethal to chronic sublethal to individuals and population decline (Wiese and Robertson, 2004WIESE, F. K. & ROBERTSON, G. J. 2004. Assessing seabird mortality from chronic oil discharges at sea. Journal of Wildlife Management, 68(3), 627-638, DOI: https://doi.org/10.2193/0022-541X(2004)068[0627:ASMFCO]2.0.CO;2
https://doi.org/10.2193/0022-541X(2004)0...
; Matcott et al., 2019MATCOTT, J., BAYLIS, S. & CLARKE, R. H. 2019. The influence of petroleum oil films on the feather structure of tropical and temperate seabird species. Marine Pollution Bulletin, 138, 135-144, DOI: https://doi.org/10.1016/j.marpolbul.2018.11.010
https://doi.org/10.1016/j.marpolbul.2018...
; Wang et al., 2021WANG, L., NABI, G., YIN, L., WANG, Y., LI, S., HAO, Z. & LI, D. 2021. Birds and plastic pollution: recent advances. Avian Research, 12(1), 59, DOI: https://doi.org/10.1186/s40657-021-00293-2
https://doi.org/10.1186/s40657-021-00293...
; Lees et al., 2022LEES, A. C., HASKELL, L., ALLINSON, T., BEZENG, S. B., BURFIELD, I. J., RENJIFO, L. M., ROSENBERG, K. V., VISWANATHAN, A. & BUTCHART, S. H. 2022. State of the world’s birds. Annual Review of Environment and Resources, 47, 231-260, DOI: https://doi.org/10.1146/annurev-environ-112420-014642
https://doi.org/10.1146/annurev-environ-...
).

Among pollutants of anthropic origin in marine ecosystems, oil is particularly problematic because it enters various compartments of the environment through daily human activities, such as sewage runoff, marine operations, drilling rigs, and pipeline spills (NRC, 2003NRC (NATIONAL RESEARCH COUNCIL). 2003. Oil in the Sea III: Inputs, Fates, and Effects. Washington: The National Academies Press, DOI: https://doi.org/10.17226/10388
https://doi.org/10.17226/10388...
; GESAMP, 2007GESAMP (Joint Group of Experts on the Scientific Aspects of Marine Environmental Protection). 2007. Estimates of Oil Entering the Marine Environment from Seabased Activities [online]. London: International Maritime Organization. Available at: http://www.gesamp.org/publications/estimates-of-oil-entering-the-marine-environment-from-sea-based-activities. [Accessed: 2019 Aug 10].
http://www.gesamp.org/publications/estim...
). Though they begin as small amounts, daily oil discharges, known as chronic hydrocarbon pollution, can have greater negative consequences than large-scale oil spill disasters (Morandin and O’Hara, 2016MORANDIN, L. A. & O’HARA, P. D. 2016. Offshore oil and gas, and operational sheen occurrence: is there potential harm to marine birds? Environmental Reviews, 24(3), 285-318, DOI: https://doi.org/10.1139/er-2015-0086
https://doi.org/10.1139/er-2015-0086...
). Oil pollution in marine ecosystems is a major threat to seabirds (García-Borboroglu et al., 2006GARCÍA-BORBOROGLU, P., BOERSMA, P. D., RUOPPOLO, V., REYES, L., REBSTOCK, G. A., GRIOT, K., HEREDIA, S. R., ADORNES, A. C. & SILVA, R. P. 2006. Chronic oil pollution harms Magellanic Penguins in the Southwest Atlantic. Marine Pollution Bulletin, 52(2), 193-198, DOI: https://doi.org/10.1016/j.marpolbul.2005.11.004
https://doi.org/10.1016/j.marpolbul.2005...
; Camphuysen, 2010CAMPHUYSEN, C. J. 2010. Declines in oil-rates of stranded birds in the North Sea highlight spatial patterns in reductions of chronic oil pollution. Marine Pollution Bulletin, 60(8), 1299-1306, DOI: https://doi.org/10.1016/j.marpolbul.2010.03.012
https://doi.org/10.1016/j.marpolbul.2010...
; Vollaard, 2017VOLLAARD, B. 2017. Temporal displacement of environmental crime: evidence from marine oil pollution. Journal of Environmental Economics and Management, 82(C), 168-180, DOI: https://doi.org/10.1016/j.jeem.2016.11.001
https://doi.org/10.1016/j.jeem.2016.11.0...
).

Despite existing in-depth knowledge on the effects of global changes on seabirds (Dias et al., 2019DIAS, M. P., MARTIN, R., PEARMAIN, E. J., BURFIELD, I. J., SMALL, C., PHILLIPS, R. A. & CROXALL, J. P. 2019. Threats to seabirds: a global assessment. Biological Conservation, 237, 525-537, DOI: https://doi.org/10.1016/j.biocon.2019.06.033
https://doi.org/10.1016/j.biocon.2019.06...
), Brazil lacks efforts to monitor the occurrence and distribution of several groups, especially pelagic birds. This is basic information to guide conservation efforts, required for fundamental questions such as which species occur in which regions, which are common or abundant, and when they occur. Systematic data collection to profile the seabird community in detail, evaluate potential impacts, and understand species predominance in certain habitats and times of the year can provide crucial information for the management and development of conservation measures for pelagic birds, including migratory species that use the Brazilian coast and that are threatened to some degree with extinction (IUCN, 2020IUCN (International Union for Conservation of Nature). 2020. Red List of Threatened Species [online]. Gland: IUCN. Available at: http://www.iucnredlist.org. [Accessed: 2021 Jan 05].
http://www.iucnredlist.org...
).

The Santos Basin is adjacent to the most densely populated area in Brazil, featuring the largest number of research institutions and universities with the highest level of knowledge of biodiversity (Calderón et al., 2014CALDERÓN, A. I., MATIAS, R. C. & LOURENÇO, H. S. 2014. Rankings na educação superior: as melhores faculdades do Brasil (1982-2000). Estudos em Avaliação Educacional, 25(57), 226-247, DOI: https://doi.org/10.18222/eae255720142830
https://doi.org/10.18222/eae255720142830...
). Even so, information on coastal and pelagic seabirds is limited and mostly focused on the coast and coastal islands, where seabird breeding colonies are located (e.g. Branco, 2003BRANCO, J. O. 2003. Reprodução das aves marinhas nas ilhas costeiras de Santa Catarina, Brasil. Revista Brasileira de Zoologia, 20(4), 619-623, DOI: https://doi.org/10.1590/S0101-81752003000400010
https://doi.org/10.1590/S0101-8175200300...
). As such, the objective of this study was to conduct a systematic (i.e. based on predefined procedures) and integrative (i.e. coupled to primary data and online sources) review of the seabird community in the Santos Basin area. We also sought to highlight the main research themes and trends carried out and relationships with threats and conservation, in order to help identify gaps in knowledge and topics of importance for research and conservation.

METHODS

Study area

The Santos Basin is the largest offshore sedimentary basin and largest producer of oil and natural gas in Brazil (Souza and Sgarbi, 2019SOUZA, L. S. & SGARBI, G. N. C. 2019. Bacia de Santos no Brasil: geologia, exploração e produção de petróleo e gás natural. Boletín de Geología, 41(1), 175-195, DOI: https://doi.org/10.18273/revbol.v41n1-2019009
https://doi.org/10.18273/revbol.v41n1-20...
). The Santos Basin occupies approximately 350,000 km2 of the southeastern-southern Brazilian coast, between 23° and 28°S, bordered to the north by the Campos Basin, marked by the Cabo Frio High off Cabo de São Tomé (22.1°S and 41°W), and to the south by the Pelotas Basin, marked by the Florianópolis High off Cabo de Santa Marta (28.55°S and 48.47°W) (Moreira et al., 2007MOREIRA, J. L. P., MADEIRA, C. V., GIL, J. A. & MACHADO, M. A. P. 2007. Bacia de Santos. Boletim de Geociências da Petrobras, 15(2), 531-549.; Gamboa et al., 2008GAMBOA, L. A. P., MACHADO, M. A. P., SILVEIRA, D. P., FREITAS, J. T. R. & SILVA, S. R. P. 2008. Evaporitos estratificados no Atlântico Sul. In: MOHRIAK, W. U., SZATMARI, P. & ANJOS, S. (eds.). Sal: Geologia e Tectônica. Exemplos nas Bacias Brasileiras. São Paulo: Beca Edições, pp. 91-163.). Thus, the four Brazilian states (Rio de Janeiro, São Paulo, Paraná, and Santa Catarina) and their offshore geopolitical boundaries were considered when assessing the occurrence of species (Figure 1). The region is also important for other socioeconomic activities such as steel mining, naval and port activities, fishing, tourism, civil construction, and commerce (Johnsson and Ikemoto, 2015JOHNSSON, R. M. F. & IKEMOTO, S. 2015. Diagnóstico do Setor Costeiro da Baía da Ilha Grande: Subsídios à Elaboração do Zoneamento Ecológico-econômico Costeiro [online]. Rio de Janeiro: INEA (Instituto Estadual do Ambiente). Available at: http://www.inea.rj.gov.br/cs/groups/public/documents/document/zwew/mdcz/~edisp/inea0073532.pdf. [Accessed: 2019 Aug 10].
http://www.inea.rj.gov.br/cs/groups/publ...
; Viana and Marum, 2020VIANA, M. A. & MARUM, V. D. O. 2020. Urban impacts of the oil and gas production chain: a case study in Santos, state of São Paulo. Cadernos Metrópole, 22(48), 617-644, DOI: https://doi.org/10.1590/2236-9996.2020-4813
https://doi.org/10.1590/2236-9996.2020-4...
).

Figure 1
Map of the study area including the offshore geopolitical limits of the Santos Basin, Brazil, and the seabird sampling transects carried out from on-board platform observations (LAATM/FURG database). Bathymetric lines at 20 m and 200 m, and the limits of the Brazilian states that are part of the Santos Basin: Rio de Janeiro (RJ), São Paulo (SP), Paraná (PR) and Santa Catarina (SC).

Systematic review

The bibliographic survey on seabirds in the Santos Basin was carried out using the ISI Web of Science, Google Scholar, and Scielo databases, which provide a multitude of academic studies (undergraduate, master’s, and doctoral theses, disser tations, and monographs) and publications in national and international journals. In the absence of other sources of information, abstracts from scientific events were used. Because the quality of the material gathered in different databases varies (see Gusenbauer and Haddaway, 2020GUSENBAUER, M. & HADDAWAY, N. R. 2020. Which academic search systems are suitable for systematic reviews or meta-analyses? Evaluating retrieval qualities of Google Scholar, PubMed, and 26 other resources. Research Synthesis Methods, 11(2), 181-217, DOI: https://doi.org/10.1002/jrsm.1378
https://doi.org/10.1002/jrsm.1378...
), our analysis of content and information within each study was checked for further quantitative analyses, and critical discussion was provided when necessary.

The search for bibliography occurred from June 2019 to July 2021, using keywords separately and in combinations that were related to seabirds and marine birds (e.g. seabirds AND diet AND São Paulo). We used keywords in both English and Portuguese, such as bycatch, fisheries, fishing, occurrence, diet, foraging ecology, migration, southeastern Brazil, albatrosses, petrels, breeding population, threats, Santos Basin, Santa Catarina (SC), Paraná (PR), São Paulo (SP), Rio de Janeiro (RJ), Brazil, and Southeastern. The three orders (Charadriiformes, Procellariiformes, and Suliformes) that include occurrences of well-known species for the Santos Basin were also used as keywords. Specific genera such as Sterna spp., Phaethon spp., Fregetta spp., Pelagodroma spp., Pterodroma spp., Pachyptila spp., and Morus spp. were used as combined keywords in order to find new documentable records for species with either limited evidences or potential occurrence in the area. This strategy also sought to locate records of offshore distribution (e.g. migration) in the Santos Basin area.

Additionally, we conducted backward citation search by checking each mention of seabird species in the national list (Pacheco et al., 2021PACHECO, J. F., SILVEIRA, L. F., ALEIXO, A., AGNE, C. E., BENCKE, G. A., BRAVO, G. A., BRITO, G. R. R., COHN-HAFT, M., MAURÍCIO, G. N., NAKA, L. N., OLMOS, F., POSSO, S., LEES, A. C., FIGUEIREDO, L. F. A., CARRANO, E., GUEDES, R. C., CESARI, E., FRANZ, I., SCHUNCK, F. & PIACENTINI, V. Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee – second edition. Ornithology Research, 29(2), 94-105, DOI: https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
) and the state lists of SC and RJ (online lists), PR (Scherer-Neto et al., 2011SCHERER-NETO, P., STRAUBE, F. C., CARRANO, E. & URBEN-FILHO, A. 2011. Lista das aves do Paraná. Hori Cadernos Técnicos, 2, 1-130.), and SP (Silveira and Uezu, 2011SILVEIRA, L. F. & UEZU, A. 2011. Checklist das aves do estado de São Paulo, Brasil. Biota Neotropical, 11(Suppl 1), 83-110, DOI: https://doi.org/10.1590/S1676-06032011000500006
https://doi.org/10.1590/S1676-0603201100...
) to identify bibliographic records for the Santos Basin region. The LAATM/FURG bibliographic database (1904–2013) was also checked. Finally, references cited in manuscripts were analyzed to locate occasional sources that did not appear through database searches.

The inclusion criteria for bibliographic sources considered references indicating the occurrence of species within the defined limits of the Santos Basin. Species living in the open sea and around oceanic islands that, therefore, use marine food resources and nest on islands were considered typical and constant components of the emerged coastal ecosystem. All species in the orders Phaethontiformes, Sphenisciformes, Procellariiformes, and Suliformes were considered seabirds, while for Charadriiformes species, only Chionidae, Stercorariidae, and Laridae (including gulls, terns, noddies, and skimmers) were included as marine. Consequently, shorebirds, or those predominantly terrestrial, from the limnetic zone of beach environments (e.g. waders, shorebirds, herons, ibises, oystercatcher), from the Charadriiformes and Pelecaniiformes orders, were not included.

After the bibliographic sources were included into the database, a systematic analysis was performed, which consisted of categorizing each publication according to: reference code; author(s); year of publication; title of the paper; species recorded in the paper; theme of the paper; Brazilian state(s) of occurrence; geographic position of the species recorded or place of coverage of the paper. Finally, we also discussed records with probable occurrence, nomenclatural changes, and identification issues regarding species cited for the area and with either unknown or lacking documentary evidence.

Integrative approach

In addition to publications found in online databases, other data sources were used to compose the list of seabird species occurring in the Santos Basin (Figure 1). We consolidated occurrence data (species presence) from three projects from the database of the Laboratório de Aves Aquáticas e Tartarugas Marinhas from the Federal University of Rio Grande - LAATM/ FURG: i) Projeto de Caracterização Regional da Bacia de Santos (PCR-BS) (the seabird survey was part of the Santos Project – The Santos Basin Regional Environmental Characterization (PCR-BS) – coordinated by PETROBRAS), carried out together with the Projeto de Monitoramento de Cetáceos na Bacia de Santos (PMC-BS) from 2019 to 2021; ii) Projeto Talude/FURG; and iii) Projeto Pro-Trindade/ FURG. The latter two were both conducted between 2009–2015 (Figure 1). These projects contain data from systematic samplings (see sampling transects in Figure 1) conducted on vessels by on-board observers, covering areas in the Santos Basin. Thus, the database is standardized for the three research projects, and their results were obtained applying the following methods: ship followers, continuous counts, and snapshot counts with on-board observers (see Daudt et al., 2019DAUDT, N. W., MARTINS, S. P., KIRINUS, E. P. & BUGONI, L. 2019. Seabird assemblage at the mouth of the Amazon River and its relationship with environmental characteristics. Journal of Sea Research, 155, 101826, DOI: https://doi.org/10.1016/j.seares.2019.101826
https://doi.org/10.1016/j.seares.2019.10...
).

In addition, the online lists published in the technical reports of the Projeto de Monitoramento de Praias (PMP-BS) (2015– 2021) and Monitoramento de Impactos de Plataformas e Embarcações sobre a Avifauna da Bacia de Santos (PMAVE) (2014–2020) were also reviewed and included in the integrative approach. PMP data were obtained from the SIMBA (Aquatic Biota Monitoring Information System) data repository and PMAVE data were extracted from the Annual Reports, available on the project website. Both PMP and PMAVE are also results of environmental licensing processes of PETROBRAS activities in the Santos Basin, whose data are available for consultation in online reports.

To spatially visualize the coverage of records obtained from bibliographic sources and data on species occurrence (presence) from the systematic data of LAATM/FURG, all geographic positions (latitude/longitude) per species or region of coverage referred to in the studies were identified. The taxonomic order of species and occurrence status in Brazil were based on Pacheco et al. (2021)PACHECO, J. F., SILVEIRA, L. F., ALEIXO, A., AGNE, C. E., BENCKE, G. A., BRAVO, G. A., BRITO, G. R. R., COHN-HAFT, M., MAURÍCIO, G. N., NAKA, L. N., OLMOS, F., POSSO, S., LEES, A. C., FIGUEIREDO, L. F. A., CARRANO, E., GUEDES, R. C., CESARI, E., FRANZ, I., SCHUNCK, F. & PIACENTINI, V. Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee – second edition. Ornithology Research, 29(2), 94-105, DOI: https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
, while the threat status of each species was classified under global (IUCN, 2020IUCN (International Union for Conservation of Nature). 2020. Red List of Threatened Species [online]. Gland: IUCN. Available at: http://www.iucnredlist.org. [Accessed: 2021 Jan 05].
http://www.iucnredlist.org...
) and national (MMA, 2022MMA (Ministério do Meio Ambiente). 2022. Portaria MMA No. 148, 7 de Junho de 2022. Lista Nacional de Espécies Ameaçadas de Extinção. Brasília: MMA.) lists. Finally, we divided species into “coastal” and “pelagic” based on the criteria defined by Croxall et al. (2012)CROXALL, J. P., BUTCHART, S. H., LASCELLES, B., STATTERSFIELD, A. J., SULLIVAN, B., SYMES, A. & TAYLOR, P. 2012. Seabird conservation status, threats and priority actions: a global assessment. Bird Conservation International, 22(1), 1-34, DOI: https://doi.org/10.1017/S0959270912000020
https://doi.org/10.1017/S095927091200002...
.

RESULTS

Systematic review

Based on the criteria established for this study, a total of 156 studies were analyzed, including publications between 1914 and 2021, all with coverage areas in the Santos Basin. An increase in the number of publications was observed after 2000 (> 80% of studies compiled), with the greatest number published in 2010 (n = 14) (Figure 2). Santa Catarina (56%) was the state with the highest number of publications, while the states of São Paulo and Rio de Janeiro accounted for 40% and 37% of studies surveyed, respectively. The state of Paraná had only 28% of publications analyzed. Among the total number of publications, only six were categorized at the national level, i.e., without a specific state defined within the basin, but with an indication of species occurrence in the area of the Santos Basin (Table S1).

Figure 2
Number of publications over the last decades with records of seabirds in the Santos Basin area, Brazil.

Regarding subjects studied, “Notes and records” (27%) and “Population and community structure” (22%) were the categories with the highest number of publications, while “Fishing” appeared in 11% of publications (Figure 3). Other anthropic impacts were recorded in only 7% of the references analyzed, including metal pollution, persistent organic pollutants, and marine litter. Other categories were recorded at < 6%, demonstrating that several areas of knowledge still lack research efforts, and several species remain without detailed studies within the Santos Basin. The majority of subjects covered were recorded in the four states, except for studies on breeding biology and health studies, which were addressed only in the states of Paraná and Santa Catarina.

Figure 3
Proportion of researched topics involving seabirds, categorized based on the main objective of each publication analyzed.

The Santos Basin contains 76 seabird species (Table S1), which represents 76% of the seabird species recorded in Brazil, according to Nunes et al. (2023)NUNES, G. T., EFE, M. A., SERAFINI, P. P. & BUGONI, L. 2023. Aves marinhas no Brasil: ações para a conservação. Oecologia Australis. [in press]. Among these, Procellariiformes was the most representative order (51%) and includes 14 species categorized under some degree of threat, either globally or nationally. Among these, Diomedea exulans, Pterodroma arminjoniana, and Puffinus lherminieri are classified as “critically endangered” at a national level, and Diomedea dabbenena is listed as “critically endangered” in both national (MMA, 2022MMA (Ministério do Meio Ambiente). 2022. Portaria MMA No. 148, 7 de Junho de 2022. Lista Nacional de Espécies Ameaçadas de Extinção. Brasília: MMA.) and global (IUCN, 2020IUCN (International Union for Conservation of Nature). 2020. Red List of Threatened Species [online]. Gland: IUCN. Available at: http://www.iucnredlist.org. [Accessed: 2021 Jan 05].
http://www.iucnredlist.org...
) lists. For the Suliformes, of the five species recorded for the Santos Basin, only Morus capensis is classified as “endangered” at the international level (Table S1).

The highest number of species was recorded for the state of São Paulo (n = 61; 80%) and were predominantly pelagic (70%) (Table 1). The states of Rio de Janeiro and Santa Catarina had 56 (74%) and 57 (75%) species, respectively, also with a predominance of pelagic seabirds (Table 1). Paraná was the state with the lowest number of seabirds recorded in the bibliographic sources (66%) and the lowest number of coastal species (n = 9) (Table 1).

Table 1
Number of species extracted from the bibliography and seabirds’ features by state bordering the Santos Basin. Classification into coastal and pelagic is based on Croxall et al. (2012)CROXALL, J. P., BUTCHART, S. H., LASCELLES, B., STATTERSFIELD, A. J., SULLIVAN, B., SYMES, A. & TAYLOR, P. 2012. Seabird conservation status, threats and priority actions: a global assessment. Bird Conservation International, 22(1), 1-34, DOI: https://doi.org/10.1017/S0959270912000020
https://doi.org/10.1017/S095927091200002...
. Status of occurrence are resident species, i.e. with breeding populations in Brazil or visitor/vagrant from Southern or Northern Hemispheres according with Pacheco et al. (2021)PACHECO, J. F., SILVEIRA, L. F., ALEIXO, A., AGNE, C. E., BENCKE, G. A., BRAVO, G. A., BRITO, G. R. R., COHN-HAFT, M., MAURÍCIO, G. N., NAKA, L. N., OLMOS, F., POSSO, S., LEES, A. C., FIGUEIREDO, L. F. A., CARRANO, E., GUEDES, R. C., CESARI, E., FRANZ, I., SCHUNCK, F. & PIACENTINI, V. Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee – second edition. Ornithology Research, 29(2), 94-105, DOI: https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
. The features of each species are described in Table S1.

There are a few species with a single record in each state, such as Aptenodytes patagonicus, Bulweria bulwerii, Chlidonias niger, Halobaena caerulea, Onychoprion fuscatus, and Phaethon aethereus for the state of Rio de Janeiro; Anous minutus, Lugensa brevirostris, and Phaetusa simplex for the state of São Paulo; Chionis albus and Thalassarche cauta for Paraná; and Larus atlanticus, Morus serrator, and Pterodroma lessonii for Santa Catarina (Table S1). Some of these are considered vagrant species (e.g. H. caerulea and L. brevirostris). The presence of migrants, including visitor and vagrant species, predominated in the four states of the Santos Basin (Table 1).

Southern visitors (39%), such as large skuas (Stercorarius spp.), albatrosses (e.g. Thalassarche spp.), and petrels/shearwaters (e.g. Procellaria spp., Pterodroma spp., and Ardenna spp.) are frequently found along the Brazilian coast and were widely recorded in the Santos Basin. In turn, species from the Northern Hemisphere, i.e. ‘visitors’ from the North (17%), and from Europe, i.e. visitors from Europe (12%), were reported in lower proportions but were also commonly recorded using the coast and pelagic regions of the Santos Basin (Table S1). Resident species, i.e. those breeding in Brazil (28%), such as Larus dominicanus, Sula leucogaster, and Fregata magnificens, were reported in the highest number of publications, with over 40 papers in the various study subjects (Table S1).

Integrative approach

While the literature review resulted in predominantly coastal or neritic studies, the integration of different databases - bibliographic and primary sources with unpublished data – allowed us to broaden the geographic cover of seabird species in the Santos Basin. Thus, a spatial cover toward offshore regions was verified. Through systematic monitoring conducted aboard vessels, it was possible to visualize the association of the most abundant species with certain habitats (Figure 4). The two most common albatross species Thalassarche chlororhynchos and Thalassarche melanophris, both migrants from the Southern Hemisphere (Figure 4), occur widely in the study region, but with marked differences in use of the region: while T. chlororhynchos is distributed across the study area, T. melanophris predominated in the southern areas of the Santos Basin, where waters are colder. This habitat segregation was also observed for Procellaria aequinoctialis, recorded frequently and in high numbers over the continental shelf and slope in the southern part of the basin, and P. conspicillata, which predominated in the shelf break/slope and pelagic areas, distributed across the study area (Figure 4). Calonectris borealis and Ardenna gravis (Figure 4), migrants from the Northern and Southern Hemisphere, respectively, were predominantly recorded in deep waters of the Santos Basin. In turn, resident seabirds (i.e. F . magnificens and S. leucogaster), which breed on Brazilian islands, were recorded both in the bibliographic sources and in the systematic censuses (LAATM/FURG) (Figure 4). Both species were registered on the continental shelf, including few records on the slope and pelagic region.

Figure 4
Occurrence (presence) of the most abundant species recorded from systematic monitoring onboard offshore vessels (LAATM/FURG database). Brazilian states: Rio de Janeiro (RJ), São Paulo (SP), Paraná (PR) and Santa Catarina (SC).

A total of 393 georeferenced locations were used from the publications analyzed (Figure 5), which covered most of the coastal areas of the four states belonging to the Santos Basin, with occasional records in the slope region. Besides these, 1,383 georeferenced occurrences were used from the LAATM/FURG dataset (Figure 5). A greater geographical cover of the basin was observed by pooling together these different sources.

Figure 5
Spatial distribution of the bibliographic sources (orange triangles) and primary data (green triangles) obtained in standardized counts onboard vessels in the LAATM/FURG database. Brazilian states: Rio de Janeiro (RJ), São Paulo (SP), Paraná (PR) and Santa Catarina (SC).

Seven seabird species were recorded by PMAVE, which were sighted from the Maritime Units of oil and natural gas production, including Anous stolidus, a tropical species that breeds on Trindade Island (Mancini et al., 2016MANCINI, P. L., SERAFINI, P. P. & BUGONI, L. 2016. Breeding seabird populations in Brazilian oceanic islands: historical review, update and a call for census standardization. Revista Brasileira de Ornitologia, 24(2), 94-115, DOI: https://doi.org/10.1007/BF03544338
https://doi.org/10.1007/BF03544338...
), the southernmost breeding location in Brazil located eastward of the Santos Basin. Through the beach monitoring database (PMP-BS), 47 species were recorded, mostly dead specimens found on the beach and thus with uncertain oceanographic distribution (Table S1). These records obtained through different techniques and from different areas of the Santos Basin allow for confirmation of the species in the region.

DISCUSSION

In this review, 156 publications on seabirds in the Santos Basin were identified, which resulted in the confirmation of the occurrence of 76 seabird species in the area. Other studies conducted on the Brazilian coast in the Campos (Lima et al., 2017LIMA, L. M., RENNÓ, B., TAVARES, D. C. & REIS, E. C. 2017. Aves marinhas da região centro-norte fluminense: riqueza, composição, distribuição, sazonalidade e conservação. In: REIS, E. C. & CURBELO-FERNANDEZ, M. P. (eds.). Mamíferos, Quelônios e Aves: Caracterização Ambiental Regional da Bacia de Campos, Atlântico Sudoeste. Rio de Janeiro: Elsevier-Habitats, v. 7, pp. 161-187, DOI: https://doi.org/10.1016/B978-85-352-7661-9.50007-5
https://doi.org/10.1016/B978-85-352-7661...
) and Sergipe-Alagoas (Almeida et al., 2019ALMEIDA, B. J. M., MOREIRA, A. C., BORGES, J. C. G., BATISTA, R. L. G., PARENTE, J. E. V. & REIS, E. C. 2019. Aves marinhas e costeiras da Bacia de Sergipe-Alagoas [online]. In: REIS, E. C. & CARNEIRO, M. E. R. (eds.). Quelônios, Aves e Mamíferos da Bacia Sergipe-Alagoas. São Cristóvão: UFS (Editora Universidade Federal de Sergipe), pp. 71-111. Available at: https://www.livraria.ufs.br/produto/quelonios-aves-e-mamiferos-marinhos-da-bacia-de-sergipe-alagoas/. [Accessed: 2019 Aug 10].
https://www.livraria.ufs.br/produto/quel...
) Basins recorded 43 and 37 seabird species, respectively. The Santos Basin is larger than these other basins, in addition to having been subject to systematic surveys at sea involving substantial sampling effort related to environmental licensing processes and research projects. In addition, an extensive list of previous studies explains the higher number of species recorded. However, different size of basins, sampling efforts, and methods allow for rudimentary comparisons, at best. Moreover, the Santos Basin is an important transition area for species from the Northern (e.g. Sterna paradisaea) and Southern (e.g. Thalassarche spp.) Hemispheres and migrants from Europe, Africa (e.g. C. borealis), and Oceania (e.g. D. epomophora and T. cauta) (Olmos et al., 1995; Olmos, 2002OLMOS, F. 2002. Non-breeding seabirds in Brazil: a review of band recoveries. Ararajuba, 10(1), 31-42.; Olmos and Bugoni, 2006OLMOS, F. & BUGONI, L. 2006. Agregações de aves marinhas associadas à pesca de espinhel-de-fundo na região sudeste-sul do Brasil. In: NEVES, T., BUGONI, L. & ROSSI-WONGTSCHOWSKI, C. L. B. (eds.). Aves Oceânicas e Suas Interações com a Pesca na Região Sudeste-Sul do Brasil. São Paulo: USP-REVIZEE, pp. 69-82.; Egevang et al., 2010EGEVANG, C., STENHOUSE, I. J., PHILLIPS, R. A., PETERSEN, A., FOX, J. W. & SILK, J. R. 2010. Tracking of Arctic Terns Sterna paradisaea reveals longest animal migration. Proceedings of the National Academy of Sciences of the United States of America, 107(5), 2078-2081, DOI: https://doi.org/10.1073/pnas.0909493107
https://doi.org/10.1073/pnas.0909493107...
; Mestre et al., 2010MESTRE, L. A. M., ROOS, A. L. & NUNES, M. F. 2010. Análise das recuperações no Brasil de aves anilhadas no exterior entre 1927 e 2006. Ornithologia, 4(1), 15-35.; Silveira and Uezu, 2011SILVEIRA, L. F. & UEZU, A. 2011. Checklist das aves do estado de São Paulo, Brasil. Biota Neotropical, 11(Suppl 1), 83-110, DOI: https://doi.org/10.1590/S1676-06032011000500006
https://doi.org/10.1590/S1676-0603201100...
; Dias et al., 2012DIAS, R. A., AGNE, C. E., BARCELOS-SILVEIRA, A. & BUGONI, L. 2012. New records and a review of the distribution of the Arctic Tern Sterna paradisaea Pontoppidan, 1763 (Aves: Sternidae) in Brazil. Check List, 8(3), 563-567, DOI: https://doi.org/10.15560/8.3.563
https://doi.org/10.15560/8.3.563...
). Many of these species occur in the area seasonally in search of food, or throughout the year, such as T . chlororhynchos, which has been recorded in all four states investigated and was the most studied albatross in the region (e.g. Harris and Hansen, 1974HARRIS, M. P. & HANSEN, L. 1974. Sea bird transects between Europe and Rio Plate, South America, in Autumm 1973. Dansk Ornitologisk Forenings Tidsskrift, 68(3-4), 117-137.; Barbieri et al., 2019BARBIERI, E., ROSELLI, L. Y. & RODRIGUES-FILHO, J. L. 2019. Influência de fatores oceanográficos sob as comunidades de aves marinhas da região de Vitória-Trindade, Banco de Abrolhos e Ressurgência Cabo Frio. In: FREITAS, R. M. (ed.). Ciências Biológicas, Campo Promissor para Pesquisa 2. São Paulo: Atena, pp. 190-210, DOI: https://doi.org/10.22533/at.ed.82619131121
https://doi.org/10.22533/at.ed.826191311...
). On the other hand, the albatross T. cauta, from the Southern Hemisphere, is considered vagrant into the Brazilian territory (Costa et al., 2011COSTA, E. S., AYALA, L., IVAR-DO-SUL, J. A., CORIA, N. R., SANCHEZ-SCAGLIONI, R. E., ALVES, M. A., PETRY, M. V. & PIEDRAHITA, P. 2011. Antarctic and sub-Antarctic seabirds in South America: a review. Oecologia Australis, 15(1), 59-68, DOI: https://doi.org/10.4257/oeco.2011.1501.06
https://doi.org/10.4257/oeco.2011.1501.0...
; Scherer-Neto et al., 2011SCHERER-NETO, P., STRAUBE, F. C., CARRANO, E. & URBEN-FILHO, A. 2011. Lista das aves do Paraná. Hori Cadernos Técnicos, 2, 1-130.).

In general, large seabirds, particularly albatrosses and petrels (e.g. Thalassarche sp., Diomedea sp., and Pterodroma sp.), are increasingly threatened and rank among birds with the highest threat risk (Butchart et al., 2004BUTCHART, S. H. M., STATTERSFIELD, A. J., BENNUN, L. A., SHUTES, S. M., AKÇAKAYA, H. R., BAILLIE, J. E. M., STUART, S. N., HILTON-TAYLOR, C. & MACE, G. M. 2004. Measuring global trends in the status of biodiversity: red list indices for birds. PLoS Biology, 2(12), e383, DOI: https://doi.org/10.1371/journal.pbio.0020383
https://doi.org/10.1371/journal.pbio.002...
; Dias et al., 2019DIAS, M. P., MARTIN, R., PEARMAIN, E. J., BURFIELD, I. J., SMALL, C., PHILLIPS, R. A. & CROXALL, J. P. 2019. Threats to seabirds: a global assessment. Biological Conservation, 237, 525-537, DOI: https://doi.org/10.1016/j.biocon.2019.06.033
https://doi.org/10.1016/j.biocon.2019.06...
). International recommendations include collecting additional information, particularly during juvenile and non-breeding periods, and analyzing threat patterns and trends (BirdLife International, 2004BIRDLIFE INTERNATIONAL. 2004. Tracking Ocean Wanderers: the Global Distribution of Albatrosses and Petrels. Results from the Global Procellariiform Tracking Workshop. Gordon’s Bay, South Africa, 2003 Sep 1-5. Cambridge, UK: BirdLife International, pp. 1-116.; Delord et al., 2008DELORD, K., BESSON, D., BARBRAUD, C. & WEIMERSKIRCH, H. 2008. Population trends in a community of large procellariiforms of Indian Ocean: potential effects of environment and fisheries interactions. Biological Conservation, 141(7), 1849-1856, DOI: https://doi.org/10.1016/j.biocon.2008.05.001
https://doi.org/10.1016/j.biocon.2008.05...
). In the present study, this group featured the highest number of species in the basin, including the most listed as threatened. Several studies in the area were associated with incidental capture (Bugoni et al., 2008aBUGONI, L., MANCINI, P. L. MONTEIRO, D. S., NASCIMENTO, L. & NEVES, T. S. 2008a. Seabird bycatch in the Brazilian pelagic longline fishery and a review of capture rates in the southwestern Atlantic Ocean. Endangered Species Research, 5(2-3), 137-147, DOI: https://doi.org/10.3354/esr00115
https://doi.org/10.3354/esr00115...
), contamination by plastics (Barbieri, 2009BARBIERI, E. 2009. Occurrence of plastic particles in procellariiforms, south of São Paulo state (Brazil). Brazilian Archives of Biology and Technology, 52(2), 341-348, DOI: https://doi.org/10.1590/s1516-89132009000200011
https://doi.org/10.1590/s1516-8913200900...
), and oil (Michels-Souza et al., 2010MICHELS-SOUZA, M. A., CRUZ, P. B. S., WALLAUER, J. & SILVA, G. S. 2010. Pinguins de Magalhães (Spheniscus magellanicus Forster, 1781) contaminados por petróleo encontrados na Ilha de Santa Catarina, Brasil. Publicações UEPG, Ciências Biológicas e da Saúde, 16(1), 29-34, DOI: https://doi.org/10.5212/Publ.Biologicas.v.16i1.0003
https://doi.org/10.5212/Publ.Biologicas....
).

The annual trend of scientific production on seabirds in the Santos Basin has increased over the last few years, similar to what was observed by Moraes-Ornellas (2009)MORAES-ORNELLAS, V. S. 2009. Uma análise de 20 anos de produção acadêmica brasileira sobre aves marinhas. Atualidades Ornitológicas [online], 152, 36-38. Available at: https://ornithologyexchange.org/resources/journals/database/ornithological-journals/atualidades-ornitol%C3%B3gicas-r36/. [Accessed: 2019 Aug 10].
https://ornithologyexchange.org/resource...
. This seems to reflect a greater interest in seabird studies associated with the increase in number of graduate courses in the region and the increase in scientific production in general in the country, as observed in all areas of knowledge and by the high number of species found in the present study in each state of the Santos Basin.

Among topics covered in the publications analyzed, the notes and records of occurrences stand out. Publications of this nature are important ornithological observation records, such as the expeditions by Murphy (1914)MURPHY, R. C. 1914. Observations on birds of the South Atlantic. Auk, 31(4), 438-457. DOI: https://doi.org/10.2307/4072006
https://doi.org/10.2307/4072006...
. Additionally, whenever a new seabird species is recorded, a note is published. Species such as P. marina (Soto et al., 2004SOTO, J. M. R., SILVA-RIBEIRO, C. C. & GUIMARÃES, M. S. D. 2004. Novo registro do Petrel-das-tormentas-de-cara-branca, Pelagodroma marina (Latham, 1790) (Procellariiformes, Hydrobatidae) na costa brasileira [online]. In: XII Congresso Brasileiro de Ornitologia (CBO). Blumenau, Santa Catarina, Brazil, 21-26 Nov 2004. Blumenau: CBO. Available at: https://ararajuba.org.br/wp-content/uploads/2020/04/3-Livro-de-resumosBlumenau-2004.pdf. [Accessed: 2019 Aug 10].
https://ararajuba.org.br/wp-content/uplo...
) and H. caerulea (Teixeira et al., 1985TEIXEIRA, D. M., NACINOVIC, J. B. & NOVELLI, R. 1985. Notes on some Brazilian seabirds. Bulletin of the British Ornithologists’ Club, 105(2), 49-51, DOI: https://doi.org/10.1111/j.1474-919X.1894.tb07768.x
https://doi.org/10.1111/j.1474-919X.1894...
), for example, were included in this survey due to a single note or record of occurrence. This highlights the importance of publishing records of seabirds of occasional occurrence, expanding knowledge of both the avifauna of the region studied and the distribution patterns of the species.

The second most commonly addressed topic in the region was population studies and bird community structures. Studies of this nature are frequent due to the presence of colonies on the coastal islands of the Santos Basin, particularly of S. leucogaster (Alves et al., 2004ALVES, V. S., SOARES, A. B. A. & COUTO, G. S. 2004. Aves marinhas e aquáticas das ilhas do litoral do estado do Rio de Janeiro. In: BRANCO, J. O. (ed.). Aves Marinhas e Insulares Brasileiras: Bioecologia e Conservação. Itajaí: Editora da UNIVALI, pp. 83-100.; Branco et al., 2010BRANCO, J. O., BARBIERI, E. & FRACASSO, H. A. A. 2010. Técnicas de pesquisa em aves marinhas. In: VON MATTER, S., STRAUBE, F. C., CÂNDIDO JUNIOR, J. F., PIACENTINI, V. & ACCORDI, I. (eds.). Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Rio de Janeiro: Editora Technical Books, pp. 219-235.), F. magnificens (Nuss et al., 2016NUSS, A., CARLOS, C. J., MORENO, I. B. & FAGUNDES, N. J. R. 2016. Population genetic structure of the Magnificent Frigatebird Fregata magnificens (Aves, Suliformes) breeding colonies in the western Atlantic Ocean. PLoS One, 11(2), e0149834, DOI: https://doi.org/10.1371/journal.pone.0149834
https://doi.org/10.1371/journal.pone.014...
), L. dominicanus (Branco and Ebert, 2002BRANCO, J. O. & EBERT, L. A. 2002. Estrutura populacional de Larus dominicanus Lichtenstein, 1823 no estuário do Saco da Fazenda, Itajaí, SC. Ararajuba, 10(1), 79-82.; Barbieri, 2008BARBIERI, E. 2008. Variação sazonal do Gaivotão (Larus dominicanus) durante o ano de 2005 no estuário de Cananéia-Iguape-Ilha Comprida, São Paulo, Brasil. Biota Neotropica, 8(2), 97-102, DOI: https://doi.org/10.1590/S1676-06032008000200011
https://doi.org/10.1590/S1676-0603200800...
; Yorio et al., 2016YORIO, P., BRANCO, J. O., LENZI, J., LUNA-JORQUERA, G. & ZAVALAGA, C. 2016. Distribution and trends in Kelp Gull (Larus dominicanus) coastal breeding populations in South America. Waterbirds, 39(spe1), 114-135, DOI: https://doi.org/10.1675/063.039.sp103
https://doi.org/10.1675/063.039.sp103...
), and, to a lesser extent, Sternidae (Efe et al., 2007EFE, M. A., AZEVEDO, M. & FILIPPINI, A. 2007. Avifauna da Estação Ecológica de Carijós, Florianópolis-SC. Ornithologia, 2(1), 1-13.; Yorio and Efe, 2008YORIO, P. & EFE, M. A. 2008. Population status of Royal and Cayenne Terns breeding in Argentina and Brazil. Waterbirds, 31(4), 561-570, DOI: https://doi.org/10.1675/1524-4695-31.4.561
https://doi.org/10.1675/1524-4695-31.4.5...
). Much of the knowledge of seabirds in the Santos Basin is with respect to coastal areas and therefore focused on these species (e.g. Spheniscus magellanicus), which have been extensively studied in relation to animal health (Martini et al., 2022MARTINI, R., MANGINI, P. R. & LANGE, R. R. 2022. Seabirds health and conservation medicine in Brazil. Journal for Nature Conservation, 69, 126238, DOI: https://doi.org/10.1016/j.jnc.2022.126238
https://doi.org/10.1016/j.jnc.2022.12623...
).

Regarding species with questionable occurrence in the Santos Basin, Puffinus assimilis was recorded by PMP and by Costa et al. (2011)COSTA, E. S., AYALA, L., IVAR-DO-SUL, J. A., CORIA, N. R., SANCHEZ-SCAGLIONI, R. E., ALVES, M. A., PETRY, M. V. & PIEDRAHITA, P. 2011. Antarctic and sub-Antarctic seabirds in South America: a review. Oecologia Australis, 15(1), 59-68, DOI: https://doi.org/10.4257/oeco.2011.1501.06
https://doi.org/10.4257/oeco.2011.1501.0...
but is listed only in the Brazilian tertiary list, recently updated by Pacheco et al. (2021)PACHECO, J. F., SILVEIRA, L. F., ALEIXO, A., AGNE, C. E., BENCKE, G. A., BRAVO, G. A., BRITO, G. R. R., COHN-HAFT, M., MAURÍCIO, G. N., NAKA, L. N., OLMOS, F., POSSO, S., LEES, A. C., FIGUEIREDO, L. F. A., CARRANO, E., GUEDES, R. C., CESARI, E., FRANZ, I., SCHUNCK, F. & PIACENTINI, V. Q. 2021. Annotated checklist of the birds of Brazil by the Brazilian Ornithological Records Committee – second edition. Ornithology Research, 29(2), 94-105, DOI: https://doi.org/10.1007/s43388-021-00058-x
https://doi.org/10.1007/s43388-021-00058...
and, given the absence of verifiable evidence, was not included in the species list here. Similarly, there are citations of Pterodroma macroptera for the area, which are questionable and possibly refer to confusion with similar species (see Bugoni, 2006BUGONI, L. 2006. Great-winged Petrel Pterodroma macroptera in Brazil. Bulletin of the British Ornithologists’ Club, 126(1), 52-54.; Valls et al., 2021VALLS, F. C. L., TAVARES, M., FLOOD, R. L. & BUGONI, L. 2021. The status of Great-winged Petrel Pterodroma macroptera in the south-west Atlantic Ocean, with notes on separation from dark-morph Trindade Petrel P. arminjoniana. Bulletin of the British Ornithologists’ Club, 141(3), 267-275, DOI: https://doi.org/10.25226/bboc.v141i3.2021.a4
https://doi.org/10.25226/bboc.v141i3.202...
for an extensive discussion). Regarding T. chrysostoma, there are many records in the region off the southern and southeastern Brazilian coast (see Costa et al., 2011COSTA, E. S., AYALA, L., IVAR-DO-SUL, J. A., CORIA, N. R., SANCHEZ-SCAGLIONI, R. E., ALVES, M. A., PETRY, M. V. & PIEDRAHITA, P. 2011. Antarctic and sub-Antarctic seabirds in South America: a review. Oecologia Australis, 15(1), 59-68, DOI: https://doi.org/10.4257/oeco.2011.1501.06
https://doi.org/10.4257/oeco.2011.1501.0...
) and several individuals between the states of São Paulo and Santa Catarina (Sick, 1979SICK, H. 1979. Notes on some Brazilian birds. Bulletin of the British Ornithologists’ Club, 99(4), 115-120.; Rosário, 1996ROSÁRIO, L. A. 1996. As aves em Santa Catarina: Distribuição Geográfica e Meio Ambiente. Florianópolis: FATMA. Available at: http://avesdesantacatarina.com.br/quem-somos#:~:text=A%20distribui%C3%A7%C3%A3o%20geogr%C3%A1fica%20da%20esp%C3%A9cie,em%20regi%C3%B5es%20de%20mata%20densa. [Accessed: 2019 10 Aug]
http://avesdesantacatarina.com.br/quem-s...
). However, these records could be attributed to T. chlororhynchos (see Bencke et al., 2010BENCKE, G. A., DIAS, R. A., BUGONI, L., AGNE, C. E., FONTANA, C. S., MAURÍCIO, G. N. & MACHADO, D. 2010. Revisão e atualização da lista das aves do Rio Grande do Sul, Brasil. Iheringia, Série Zoologia, 100(4), 519-556, DOI: https://doi.org/10.1590/S0073-47212010000400022
https://doi.org/10.1590/S0073-4721201000...
for an extensive discussion of the confusion between these two species on the Brazilian waters). In turn, the numerous mentions of C. diomedea both in the Santos Basin and along the Brazilian coast are predominantly attributable to C. borealis, now considered a full species (see Oliveira et al., 2019OLIVEIRA, G., NUNES, G. T., MARQUES, F. P. & BUGONI, L. 2019. Scopoli’s Shearwater, Calonectris diomedea, in the southwest Atlantic Ocean. Marine Biodiversity, 49(1), 531-537, DOI: https://doi.org/10.1007/s12526-017-0798-9
https://doi.org/10.1007/s12526-017-0798-...
on the separation of species of the genus). Both C. borealis and C. diomedea surely occur in the Santos Basin. Regarding T. cauta, this species has also been separated into T. steadi, T. salvini, and T. eremita (Dellacasa et al., 2022DELLACASA, R. F., CHAVEZ, L. N. & TAMINI, L. L. 2022. Salvin’s Albatross Thalassarche salvini interacting with freezer trawlers in waters of the Patagonian Shelf. Marine Ornithology, 50(1), 99-102.), and possibly occur on Brazilian territory, but T. cauta and T. steadi are indistinguishable at sea and require genetic analysis for specific assignment (Pereira et al., 2016PEREIRA, A., DAUDT, N. W., NUSS, A., TAVARES, M. & CARLOS, C. J. 2016. The first confirmed record of the White-capped Albatross (Thalassarche steadi) in Brazil. Revista Brasileira de Ornitologia, 24(3), 286-289, DOI: https://doi.org/10.1007/BF03544355
https://doi.org/10.1007/BF03544355...
). Similarly, P . deserta had been included in the list due to unquestionable tracking data from Northern Hemisphere colonies (Ramos et al., 2017RAMOS, R., CARLILE, N., MADEIROS, J., RAMIREZ, I., PAIVA, V. H., DINIS, H. A., ZINO, F., BISCOITO, M., LEAL, G. R., BUGONI, L., JODICE, P. G. R., RYAN, P. G. & GONZÁLEZ-SOLÍS, J. 2017. It is the time for oceanic seabirds: tracking year‐round distribution of gadfly petrels across the Atlantic Ocean. Diversity and Distributions, 23(7), 794-805, DOI: https://doi.org/10.1111/ddi.12569
https://doi.org/10.1111/ddi.12569...
) and two specimens in southeastern Brazil, which are predicted to have crossed the studied area (Brusco et al., 2021BRUSCO, G. M., AMARAL, K. B., REPENNING, M., WHITTAKER, A., VICENTINI-NETO, F. L. & BUGONI, L. 2021. Gadfly petrels of the Pterodroma feae-complex in southwestern Atlantic Ocean. Ornithology Research, 29(3), 160-165, DOI: https://doi.org/10.1007/s43388-021-00066-x
https://doi.org/10.1007/s43388-021-00066...
). Other species of the P . feae-complex are expected in the area. Finally, Xema sabini was found by PMP (Prado et al., 2021PRADO, J. H., CANANI, G., CASTILHO, P. V. & DAUDT, N. W. 2021. Sabine’s Gulls Xema sabini outside of their main wintering areas are not necessarily vagrants. Marine Ornithology, 49(2), 349-357.), but the record occurred just south of the Santos Basin boundary; it was thus excluded from this review.

The relationship between fisheries and seabirds, either through the consumption of discards by birds (e.g. Branco, 2001BRANCO, J. O. 2001. Descartes da pesca do Camarão Sete-barbas como fonte de alimento para aves marinhas. Revista Brasileira de Zoologia, 18(1), 293-300, DOI: https://doi.org/10.1590/S0101-81752001000100033
https://doi.org/10.1590/S0101-8175200100...
; Carniel and Krul, 2012aCARNIEL, V. L. & KRUL, R. 2012a. Utilization of discards from small-scale fisheries by seabirds in coastal waters of Paraná state, Brazil. Seabird, 25, 29-38.,bCARNIEL, V. L. & KRUL, R. 2012b. Use of artisanal fishery discards by seabirds on the Paraná coast in Brazil. Marine Ornithology, 40(1), 57-62.), or by incidental capture (e.g. Bugoni et al., 2008aBUGONI, L., MANCINI, P. L. MONTEIRO, D. S., NASCIMENTO, L. & NEVES, T. S. 2008a. Seabird bycatch in the Brazilian pelagic longline fishery and a review of capture rates in the southwestern Atlantic Ocean. Endangered Species Research, 5(2-3), 137-147, DOI: https://doi.org/10.3354/esr00115
https://doi.org/10.3354/esr00115...
), is another important theme addressed in the publications analyzed. As visual predators, they often seek fishing vessels and/ or feed on fish discarded from fishing operations. Thus, research that follows fishing fleets also allows for the identification of associated avifauna (e.g. Olmos, 1997OLMOS, F. 1997. Seabirds attending bottom long-line fishing off southeastern Brazil. Ibis, 139(4), 685-691, DOI: https://doi.org/10.1111/j.1474-919x.1997.tb04692.x
https://doi.org/10.1111/j.1474-919x.1997...
). To some extent, seabirds benefit from fishing activity by gaining access to food resources that would otherwise be unavailable, such as demersal fish or offal of large fish (tuna, billfishes) and sharks. On the other hand, species can be captured by fishing gear; this interaction is one of the main causes of the threat levels of many species. Studies frequently investigate seabirds and their relationship to longline fishing and incidental species capture (Olmos and Bugoni, 2006OLMOS, F. & BUGONI, L. 2006. Agregações de aves marinhas associadas à pesca de espinhel-de-fundo na região sudeste-sul do Brasil. In: NEVES, T., BUGONI, L. & ROSSI-WONGTSCHOWSKI, C. L. B. (eds.). Aves Oceânicas e Suas Interações com a Pesca na Região Sudeste-Sul do Brasil. São Paulo: USP-REVIZEE, pp. 69-82.; Olmos et al., 2006OLMOS, F. & BUGONI, L. 2006. Agregações de aves marinhas associadas à pesca de espinhel-de-fundo na região sudeste-sul do Brasil. In: NEVES, T., BUGONI, L. & ROSSI-WONGTSCHOWSKI, C. L. B. (eds.). Aves Oceânicas e Suas Interações com a Pesca na Região Sudeste-Sul do Brasil. São Paulo: USP-REVIZEE, pp. 69-82.; Bugoni et al., 2008aBUGONI, L., MANCINI, P. L. MONTEIRO, D. S., NASCIMENTO, L. & NEVES, T. S. 2008a. Seabird bycatch in the Brazilian pelagic longline fishery and a review of capture rates in the southwestern Atlantic Ocean. Endangered Species Research, 5(2-3), 137-147, DOI: https://doi.org/10.3354/esr00115
https://doi.org/10.3354/esr00115...
; Bugoni et al., 2009BUGONI, L., D’ALBA, L. & FURNESS, R. W. 2009. Marine habitat use of wintering Spectacled Petrels Procellaria conspicillata, and overlap with longline fishery. Marine Ecology Progress Series, 374, 273-285, DOI: https://doi.org/10.3354/meps07750
https://doi.org/10.3354/meps07750...
; Canani et al., 2020CANANI, G., COSTA, A. S, NEVES, T. & GIANUCA, D. 2020. Distribuição espaço-temporal de albatrozes-gigantes Diomedea spp. associados a pescarias de espinhel pelágico no sul e sudeste do Brasil. Ornithologia, 11(1), 16-22.). The Santos Basin is a region with intense fishing activity (e.g. Sales et al., 2008SALES, G., GIFFONI, B. B. & BARATA, P. C. 2008. Incidental catch of sea turtles by the Brazilian pelagic longline fishery. Journal of the Marine Biological Association of the United Kingdom, 88(4), 853-864, DOI: https://doi.org/10.1017/S0025315408000441
https://doi.org/10.1017/S002531540800044...
; Canani et al., 2020CANANI, G., COSTA, A. S, NEVES, T. & GIANUCA, D. 2020. Distribuição espaço-temporal de albatrozes-gigantes Diomedea spp. associados a pescarias de espinhel pelágico no sul e sudeste do Brasil. Ornithologia, 11(1), 16-22.) that receives migratory species, some listed as “critically endangered” (e.g. D. dabbenena, D. exulans), which demonstrates the importance of studies addressing threats and conservation issues.

However, few studies addressed the relationship between seabirds and oceanographic processes in the Santos Basin, for example by using tracking (e.g. Bugoni et al., 2009BUGONI, L., D’ALBA, L. & FURNESS, R. W. 2009. Marine habitat use of wintering Spectacled Petrels Procellaria conspicillata, and overlap with longline fishery. Marine Ecology Progress Series, 374, 273-285, DOI: https://doi.org/10.3354/meps07750
https://doi.org/10.3354/meps07750...
) or bird counts at sea (e.g. Neves et al., 2006NEVES, T., VOOREN, C. M., BUGONI, L., OLMOS, F. & NASCIMENTO, L. 2006. Distribuição e abundância de aves marinhas no sudeste-sul do Brasil. In: NEVES, T., BUGONI, L. & ROSSI-WONGTSCHOWSKI, C. L. B. (eds.). Aves Oceânicas e Suas Interações com a Pesca na Região Sudeste-Sul do Brasil. São Paulo: USP-REVIZEE, pp. 11-36.). Monitoring avifauna through systematic observation aboard vessels is costly and time-consuming but necessary to accurately establish abundance and distribution of bird species at sea. In turn, beach monitoring (e.g. PMP), which collects and studies carcasses of birds, allows us to identify species that occur in the region and sample tissues, as well as to study anthropic impacts (e.g. Michels-Souza et al., 2010MICHELS-SOUZA, M. A., CRUZ, P. B. S., WALLAUER, J. & SILVA, G. S. 2010. Pinguins de Magalhães (Spheniscus magellanicus Forster, 1781) contaminados por petróleo encontrados na Ilha de Santa Catarina, Brasil. Publicações UEPG, Ciências Biológicas e da Saúde, 16(1), 29-34, DOI: https://doi.org/10.5212/Publ.Biologicas.v.16i1.0003
https://doi.org/10.5212/Publ.Biologicas....
; Moura et al., 2018MOURA, J. F., TAVARES, D. C., LEMOS, L. S., ACEVEDO-TREJOS, E., SAINT’PIERRE, T. D., SICILIANO, S. & MERICO, A. 2018. Interspecific variation of essential and non-essential trace elements in sympatric seabirds. Environmental Pollution, 242(Pt A), 470-479, DOI: https://doi.org/10.1016/j.envpol.2018.06.092
https://doi.org/10.1016/j.envpol.2018.06...
), contamination by petroleum (e.g. Barbieri, 2009BARBIERI, E. 2009. Occurrence of plastic particles in procellariiforms, south of São Paulo state (Brazil). Brazilian Archives of Biology and Technology, 52(2), 341-348, DOI: https://doi.org/10.1590/s1516-89132009000200011
https://doi.org/10.1590/s1516-8913200900...
; Michels-Souza et al., 2010MICHELS-SOUZA, M. A., CRUZ, P. B. S., WALLAUER, J. & SILVA, G. S. 2010. Pinguins de Magalhães (Spheniscus magellanicus Forster, 1781) contaminados por petróleo encontrados na Ilha de Santa Catarina, Brasil. Publicações UEPG, Ciências Biológicas e da Saúde, 16(1), 29-34, DOI: https://doi.org/10.5212/Publ.Biologicas.v.16i1.0003
https://doi.org/10.5212/Publ.Biologicas....
), and impacts to animal health (Niemeyer, 2014NIEMEYER, C. 2014. Investigação de enfermidades virais selecionadas em aves marinhas da Costa Atlântica da América do Sul. DSc. São Paulo: USP (Universidade de São Paulo), DOI: https://doi.org/10.11606/T.10.2014.tde-25082015-143241
https://doi.org/10.11606/T.10.2014.tde-2...
; Ebert et al., 2016EBERT, L. A., SCHLEMPER, J. C., PELISSER, M. R., PEREIRA, B. A., SILVA, M. A. C. & BRANCO, J. O. 2016. Pathogenic bacteria associated with Kelp Gull Larus dominicanus (Charadriiformes, Laridae) on the coast of Santa Catarina state – Brazil. International Journal of Current Microbiology and Applied Science, 5(5), 458-473, DOI: http://dx.doi.org/10.20546/ijcmas.2016.505.048
http://dx.doi.org/10.20546/ijcmas.2016.5...
; Fink et al., 2018FINK, D., DRUMOND, L., BASÍLIO, M. I., SARTORI, C. M., ANDRADE, T. R., SANTOS, N. Z. & CREMER, M. J. 2018. Gota úrica visceral em Bobo-pequeno (Puffinus puffinus) no sul do Brasil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 70(2), 486-490, DOI: https://doi.org/10.1590/1678-4162-9916
https://doi.org/10.1590/1678-4162-9916...
; Vanhoni et al., 2018VANHONI, M. S., ARNÁ, G. M., SPRENGER, L. K., VIEIRA, D. L, LUIS, L. W. & MOLENTO, M. B. 2018. Occurrence of gastrointestinal parasites in Spheniscus magellanicus (Foster, 1781) located in Pontal do Sul, PR, Brazil. Arquivo Brasileiro de Medicina Veterinária e Zootecnia, 70(2), 491-496, DOI: https://doi.org/10.1590/1678-4162-9335
https://doi.org/10.1590/1678-4162-9335...
; Martini et al., 2022MARTINI, R., MANGINI, P. R. & LANGE, R. R. 2022. Seabirds health and conservation medicine in Brazil. Journal for Nature Conservation, 69, 126238, DOI: https://doi.org/10.1016/j.jnc.2022.126238
https://doi.org/10.1016/j.jnc.2022.12623...
). However, studies on the spatial distribution of seabirds along the Santos Basin are scarce, be they from at-sea counts or tracking data, and are restricted to few species and to the neritic region (< 20 m depth).

CONCLUSION

Although the area sampled is limited compared to the entire Brazilian territory (along 40 degrees of latitude and 7,000 km of coastline and adjacent waters), a large number of species uses the Santos Basin for breeding, foraging, and as a migratory corridor for trans-hemispheric or intra-hemispheric movements. The combination of unpublished data obtained in the framework of the Santos Basin project and other projects through observations on at-sea platforms has satisfactorily complemented spatial gaps in bird records, especially offshore where data were especially limited. A substantial number of studies on seabirds in the Santos Basin focused on a few subjects. The number and rarity of species is well-established, and additional species probably reach the area as vagrants. The integration of information and sampling methods improves the ecological understanding of seabird species, allowing for environmental impact assessments of the activities of the offshore oil and gas industry. However, efforts to establish the abundance and distribution of seabirds across the entire Santos Basin region (both coastal and pelagic) and to understand the relationship between birds and oceanographic and meteorological characteristics were found to be scarce. Similarly, many species have not yet been the subject of specific studies in the area, abundance notwithstanding. Additionally, impact studies on fishing, contamination by marine litter and organic and inorganic pollutants, and oceanographic processes on species are still scarce. Essential topics of focus to support conservation actions going forward include the relationship between species and threats, the importance of protected areas in the basin, and demographic studies addressing population viability, connectivity, and dynamics between populations and colonies. Given the complex environmental scenario, with various threats to seabird conservation already identified and others expected in the coming years such as off-shore wind farms (Bugoni et al., 2022BUGONI, L., NUNES, G. T., LAUXEN, M. S., GOMES, C., ROOS, A. L. & SERAFINI, P. P. 2022. Eólicas offshore no Brasil: potenciais impactos, recomendações para o licenciamento e implicações para a conservação das aves marinhas e costeiras [online]. GOMES-FILHO, A. (eds.) In: CEMAVE/ICMBio (orgs.). Relatório de Áreas de Concentração de Aves Migratórias no Brasil. Cabeledo: pp. 137-180. Available at: https://www.icmbio.gov.br/cemave/images/stories/Publica%C3%A7%C3%B5es_cient%C3%ADficas/RELATORIO_MIGRATORIAS_2022_opt.pdf. [Accessed: 2022 Sep 01].
https://www.icmbio.gov.br/cemave/images/...
) and global warming (Baum and Worm, 2009BAUM, J. K. & WORM, B. 2009. Cascading top-down effects of changing oceanic predator abundances. Journal of Animal Ecology, 78(4), 699-714, DOI: https://doi.org/10.1111/j.1365-2656.2009.01531.x
https://doi.org/10.1111/j.1365-2656.2009...
), the continued assessment of seabird populations in the Santos Basin and impact mitigation and prevention is necessary.

ACKNOWLEDGMENTS

We thank Petrobras for the possibility of collecting and analyzing material through the PD&I investment clauses of the Agência Nacional do Petróleo, Gás Natural e Biocombustíveis do Brasil (oil & gas regulatory agency, ANP) through the Santos Project – Santos Basin Environmental Characterization (PCR-BS). We also thank Projeto de Monitoramento de Cetáceos na Bacia de Santos - PMC-BS (Cetacean monitoring project in the Santos Basin), a program required by IBAMA (federal environmental agency) for environmental licensing of oil production and transport by Petrobras in the Santos Basin, run by Socioambiental Consultores Associados and Fundação de Apoio à Universidade de São Paulo (FUSP) as management partner (Proc. No. 2017/00686-0 and 3366). The authors are also grateful to Projeto Talude at FURG, coordinators, to seabird observers who provided substantial support for the sampling presented herein, and to anonymous reviewers whose suggestions helped improve and clarify this manuscript. F.C.L.V., P.L.C., and D.R.A. received a postdoctoral scholarship granted by FUSP Petrobras/CENPES, and L.B. is a research fellow of the Conselho Nacional de Desenvolvimento Científico e Tecnológico -CNPq (Proc. No. 311409/2018-0).

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Edited by

Associate Editor: Gustavo Fonseca

Publication Dates

  • Publication in this collection
    03 Apr 2023
  • Date of issue
    2023

History

  • Received
    31 May 2022
  • Accepted
    01 Nov 2022
Instituto Oceanográfico da Universidade de São Paulo Praça do Oceanográfico 191, CEP: 05508-120, São Paulo, SP - Brasil, Tel.: (11) 3091-6501 - São Paulo - SP - Brazil
E-mail: diretoria.io@usp.br