Introduction
Emerging infectious diseases can have devastating impacts on hosts, sometimes with consequences for entire ecosystems (Machalaba et al., Reference Machalaba, Feferholtz, Uhart and Karesh2020; Nicholson et al., Reference Nicholson, Marneweck, Lindsey, Marnewick and Davies-Mostert2020; Ferreyra et al., Reference Ferreyra, Rudd, Foley, Vanstreels, Martín, Donadio and Uhart2022; Jain, Reference Jain2023). For example, the pandemic of high pathogenicity avian influenza (HPAI H5Nx) resulted in the death of over half a billion wild birds and poultry worldwide within just a few years of emergence in the early 2020s (Gamarra-Toledo et al., Reference Gamarra-Toledo, Plaza, Angulo, Gutiérrez, García-Tello, Saravia-Guevara, Mejía-Vargas, Epiquién-Rivera, Quiroz-Jiménez, Martinez, Huamán-Mendoza, Inga-Díaz, La Madrid, Luyo, Ventura and Lambertucci2023; Roberts et al., Reference Roberts, Abolnik, Waller, Shaw, Ludynia, Roberts, Kock, Makhado, Snyman and Abernethy2023; Puryear and Runstadler, Reference Puryear and Runstadler2024). Diseases can be particularly severe in areas where hosts are shielded geographically from pathogen exposure, particularly those on remote islands (Wyatt et al., Reference Wyatt, Campos, Gilbert, Kolokotronis, Hynes, DeSalle and Greenwood2008; Atkinson and LaPointe, Reference Atkinson and LaPointe2009; Vanstreels et al., Reference Vanstreels, Uhart, Work, Young and VanderWerf2023). Such threats to isolated populations are often exacerbated by anthropogenic effects, such as global connectivity and climate change, in part through effects on pathogen and vector survival, distribution and spread (Steig et al., Reference Steig, Schneider, Rutherford, Mann, Comiso and Shindell2009; Lynton-Jenkins et al., Reference Lynton-Jenkins, Russell, Chaves and Bonneaud2021). Monitoring the health and infection status of vulnerable species inhabiting remote locations can therefore be critical for their conservation.
The islands of the southwest Atlantic and Southern Ocean are home to a rich diversity of bird species, including many endemics or globally important breeding populations (Poncet et al., Reference Poncet, Wolfaardt, Barbraud, Reyes-Arriagada, Black, Powell and Phillips2020; Favero et al., Reference Favero, Seco Pon, Paz, Hernandez, Copello, Acha, Iribarne and Piola2024; Poncet et al., Reference Poncet, Wolfaardt, Black, Browning, Lawton, Lee, Passfield, Strange and Phillips2017). This includes highly threatened albatrosses and petrels, many of which are declining because of incidental mortality (bycatch) in fisheries, predation by invasive species, climate change, or degradation/loss of nesting habitat (Dias et al., Reference Dias, Martin, Pearmain, Burfield, Small, Phillips, Yates, Lascelles, Borborolu and Croxall2019; Phillips et al., Reference Phillips, Fort, Dias, Young and VanderWerf2023; Baker et al., Reference Baker, Komyakova, Wellbelove, Beynon and Haward2024). Until recently, there have been few documented cases of mass mortality on islands where albatrosses and petrels breed, but it is unclear whether this is because these populations are largely shielded from infection (Vanstreels et al., Reference Vanstreels, Uhart, Work, Young and VanderWerf2023), or because of a lack of attention to their health and disease status (Uhart et al., Reference Uhart, Gallo and Quintana2018). Avian cholera (Pasteurella multocida) is, however, thought to have caused mortality in albatrosses and petrels in the 1980s, with more recent infections in asymptomatic individuals raising questions around the reservoir potential of these species (Gamble et al., Reference Gamble, Garnier, Jaeger, Gantelet, Thibault, Tortosa, Bourret, Thiebot, Delord, Weimerskirch, Tornos, Barbraud and Boulinier2019). Overall, outbreaks of infectious diseases in albatrosses and petrels appear to be on the rise, e.g. avian cholera and Erysipelothrix rhusiopathiae cause yearly recurrent die-offs of the Indian yellow-nosed albatross (Thalassarche carteri) on Amsterdam Island (Jaeger et al., Reference Jaeger, Gamble, Lagadec, Lebarbenchon, Bourret, Tornos, Barbraud, Lemberger, Delord, Weimerskirch, Thiebot, Boulinier and Tortosa2020). In 2024, an outbreak of HPAI H5N1 on South Georgia caused mortality in multiple taxa, including wandering albatrosses (Diomedea exulans), which are listed as Vulnerable by the International Union for the Conservation of Nature, as well as brown skuas (Stercorarius antarcticus), gentoo penguins (Pygoscelis papua) and Antarctic fur seals (Arctocephalus gazella) (Bennison et al., Reference Bennison, Adlard, Banyard, Blockley, Blyth, Browne and Phillips2024). Given increasing likelihood of disease outbreaks at breeding sites (Banyard et al., Reference Banyard, Bennison and Byrne2024), the establishment of continuous monitoring programmes of albatross and petrel health is integral to the rapid detection of emerging diseases and effective predictions of disease spread based on prior infection history (Vanstreels et al., Reference Vanstreels, Uhart, Work, Young and VanderWerf2023).
Infectious pathogens at risk of emergence in seabirds breeding on remote islands include vector-borne haemosporidian parasites in the genera Plasmodium, Haemoproteus and Leucocytozoon (Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011; Parsons et al., Reference Parsons, Voogt, Schaefer, Peirce and Vanstreels2017; Vanstreels et al., Reference Vanstreels, Yabsley, Parsons, Swanepoel and Pistorius2018; Muñoz-Leal et al., Reference Muñoz-Leal, Clemes, Lopes, Acosta, Serpa, Mayorga, Gennari, González-Acuña and Labruna2019), which cause avian malaria or malaria-like diseases (Valkiunas, Reference Valkiunas2005; Palinauskas et al., Reference Palinauskas, Valkiunas, Bolshakov and Bensch2008; Bensch et al., Reference Bensch, Hellgren and Pérez‐Tris2009; Pacheco and Escalante, Reference Pacheco and Escalante2023). Infections with these parasites have been associated with increased mortality, population declines and even extinctions (Warner, Reference Warner1968; Hill et al., Reference Hill, Howe, Gartrell and Alley2010). Sublethal effects include reductions in body condition, sexual ornamentation or reproductive success, as well as prolonged stopovers or delayed migration (Martínez-Abraín et al., Reference Martínez-Abraín, Esparza and Oro2004; Marzal et al., Reference Marzal, de Lope, Navarro and Møller2005, Reference Marzal, Bensch, Reviriego, Balbontin and De Lope2008; Barbosa and Palacios, Reference Barbosa and Palacios2009; Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011; Hegemann et al., Reference Hegemann, Abril, Muheim, Sjöberg, Alerstam, Nilsson and Hasselquist2018). In seabirds, infection with Plasmodium relictum, P. circumflexum and P. vaughani has been associated with increased mortality in captive Humboldt and Magellanic penguins (Spheniscus demersus and S. magellanicus), little penguins (Eudyptula minor) and Atlantic puffins (Fratercula arctica) (Sallaberry-Pincheira et al., Reference Sallaberry-Pincheira, Gonzalez-Acuña, Herrera-Tello, Dantas, Luna-Jorquera, Frere, Valdés-Velasquez, Simeone and Vianna2015; Sijbranda et al., Reference Sijbranda, Hunter, Howe, Lenting, Argilla and Gartrell2017; Meister et al., Reference Meister, Richard, Hoby, Gurtner and Basso2021).
Other haemoparasites isolated recently from seabirds at risk of emergence include the bacteria Borrelia (Dietrich et al., Reference Dietrich, Gómez-Díaz and McCoy2011; Schramm et al., Reference Schramm, Gauthier-Clerc, Fournier, McCoy, Barthel, Postic, Handrich, Maho and Jaulhac2014; Parsons et al., Reference Parsons, Voogt, Schaefer, Peirce and Vanstreels2017; Vanstreels et al., Reference Vanstreels, Uhart, Work, Young and VanderWerf2023), Anaplasma and Ehrlichia (Anaplasmataceae) (Vanstreels et al., Reference Vanstreels, Yabsley, Parsons, Swanepoel and Pistorius2018; Muñoz-Leal et al., Reference Muñoz-Leal, Clemes, Lopes, Acosta, Serpa, Mayorga, Gennari, González-Acuña and Labruna2019). These parasites are transmitted through ticks such as Ixodes spp. and Argasidae spp., which are common in many seabird colonies (Dietrich et al., Reference Dietrich, Gómez-Díaz and McCoy2011, Reference Dietrich, Lebarbenchon, Jaeger, Le Rouzic, Bastien, Lagadec, McCoy, Pascalis, Le Corre, Dellagi and Tortosa2014; Vanstreels et al., Reference Vanstreels, Yabsley, Parsons, Swanepoel and Pistorius2018; Muñoz-Leal et al., Reference Muñoz-Leal, Clemes, Lopes, Acosta, Serpa, Mayorga, Gennari, González-Acuña and Labruna2019). Borrelia parasites have been isolated from Ixodes uriae ticks collected in colonies of razorbills (Alca torda), Atlantic puffins (F. arctica) and black-browed albatrosses (Thalassarche melanophris) (Olsen et al., Reference Olsen, Jaenson, Noppa, Bunikis and Bergström1993, Reference Olsen, Duffy, Jaenson, Gylfe, Bonnedahl and Bergström1995; Gylfe et al., Reference Gylfe, Olsen, Straševičius, Marti Ras, Weihe, Noppa and Bergström1999; Munro et al., Reference Munro, Ogden, Mechai, Lindsay, Robertson, Whitney and Lang2019). Such infections can be pathogenic in seabirds (Yabsley et al., Reference Yabsley, Parsons, Horne, Shock and Purdee2012; Parsons et al., Reference Parsons, Gous, Cranfield, Cheng, Schultz, Horne, Last, Lampen, Ludynia, Bousfield, Strauss, Peirce and Vanstreels2018; Vanstreels et al., Reference Vanstreels, Parsons, Pistorius and Schaefer2019), as evidenced by a Borrelia-positive African penguin (S. demersus) that presented antemortem neurological signs and lesions similar to those reported in an owl fatally infected with B. hermsii and a domestic fowl infected with B. anserina (Dickie and Barrera, Reference Dickie and Barrera1964; Thomas et al., Reference Thomas, Bunikis, Barbour and Wolcott2002; Bunikis et al., Reference Bunikis, Garpmo, Tsao, Berglund, Fish and Barbour2004; Yabsley et al., Reference Yabsley, Parsons, Horne, Shock and Purdee2012). Anaplasma phagocytophilum has been detected in blood samples from passerines, suggesting their potential role in transmitting the bacterium to ticks; however, the significance of wild birds in the infectious cycle of this parasite remains unclear (Pedersen et al., Reference Pedersen, Jenkins and Kjelland2020). Although only mammals have so far been confirmed as competent hosts and reservoirs for Ehrlichia bacteria (Rar and Golovljova, Reference Rar and Golovljova2011), there is growing evidence that the host range may extend to other vertebrates after the detection in wild birds in Brazil of Ehrlichiae typically associated with ungulates and carnivores (Machado et al., Reference Machado, André, Werther, de Sousa, Gavioli and Alves Junior2012).
The goal of this study was to survey vector-borne infectious diseases in albatrosses and petrels sampled in the southwest Atlantic and Southern Ocean, with the aim of detecting any novel infection, as well as establishing baselines for future surveillance. We screened 5 species of albatrosses and 12 species of petrels for the presence of haemosporidian parasites (Plasmodium, Haemoproteus and Leucocytozoon), and the bacterial pathogens Anaplasma, Ehrlichia and B. burgdorferi sensu lato (s.l.). Understanding host–pathogen interactions in these species will be key to informing conservation strategies of these threatened species and mitigating potential disease threats in a rapidly changing environment.
Materials and methods
Sampling
The samples were obtained between 2013 and 2023 from 4 different sources: (i) breeding adults and chicks at colonies on Bird Island, South Georgia (54°00′S, 38°03′W); (ii) seabirds bycaught in Brazilian fisheries; (iii) birds found in a weakened state on the Brazilian coast and taken to 2 rehabilitation centres; and (iv) seabirds monitored in stranding networks in Brazil (Table 1). Detailed fieldwork procedures, methods of sampling and locations of seabirds surveyed are provided in Supplementary Table S1.
Table 1. Albatrosses and petrels screened for vector-borne parasites from 2013 to 2023 from the southern Brazilian Coast, Brazilian fisheries and from colonies in Bird Island, South Georgia
DNA extraction and molecular analysis
A total of 96 DNA samples from the seabirds sampled in South Georgia were extracted using a QIAamp DNA Micro Kit (Qiagen, Hilden, Germany) following the manufacturer’s protocol. For all other samples (Table 1), DNA was extracted using the phenol-chloroform method (Sambrook et al., Reference Sambrook, Fritsch and Maniatis1989), with the exception of blood samples preserved in ethanol (Supplementary Table S1), which were extracted using a slightly modified approach (Maia et al., Reference Maia, Vilaça, Silva, Santos and Dantas2017). First, we tested for the presence of haemosporidians (Plasmodium, Haemoproteus and Leucocytozoon) in a subset of samples (N = 96 blood samples from South Georgia and 30 liver samples), using a nested PCR targeting a 617-bp fragment of the cytochrome b gene (Hellgreen et al., Reference Hellgreen, Waldenstrom and Bensch2004) and including DNA from Plasmodium gallinaceum strain A8 (MalAvi lineage GALLUS01), Haemoproteus majoris (MalAvi lineage PARUS1) and Leucocytozoon (MalAvi lineage PARUS22) as positive controls. Second, we tested for the presence of Borrelia burgdorferi sensu lato (s.l.) using a nested PCR, which targets the 5S–23S rRNA spacer region of all Borreliae species and the same positive controls mentioned by Newman et al. (Reference Newman, Eisen, Eisen, Fedorova, Hasty, Vaughn and Lane2015). Finally, we tested for the presence of Ehrlichia and Anaplasma in 219 tissue samples using a PCR protocol specifically designed to amplify a 345-bp fragment of the 16S rRNA gene (Parola et al., Reference Parola, Roux, Camicas, Baradji, Brouqui and Raoult2000); Anaplasma marginale DNA was used as a positive control. In all assays, we included ultrapure water as negative controls.
Light microscopy of blood smears
The 96 blood smears taken from the live seabirds at South Georgia were analysed by light microscopy, following Merino et al. (Reference Merino, Potti and Fargallo1997) and Quillfeldt et al. (Reference Quillfeldt, Martínez, Hennicke, Ludynia, Gladbach, Masello, Riou and Merino2010). In brief, one half of the slide was scanned at ×200 magnification to look for haemoparasites, and at least 20 fields in the other half at ×400 to look for intracellular stages of haematozoa. A minimum of 2000 to 10 000 erythrocytes were also checked using the oil immersion objective (1000×).
Results
None of the parasites of interest were detected in the 269 sampled seabirds (Table 1). This included no evidence of infection with either Plasmodium, Haemoproteus or Leucocytozoon parasites in the 96 samples from live albatrosses and petrels obtained in South Georgia, nor of infection with Plasmodium or Haemoproteus in the liver samples from wandering albatross chicks (18) or black-browed albatrosses (12) found dead at South Georgia or in southern Brazil. We found no evidence of infection with Borrelia spp. (Table 1) in any of the 96 samples from live albatrosses and petrels obtained in South Georgia, or with Anaplasmataceae parasites in any of the 219 tissue samples from seabirds found at the Brazilian coast or obtained as bycatch. Microscopic observations were consistent with molecular findings in that we did not detect the presence of parasitized erythrocytes in any of the 96 blood smears obtained from live wandering albatrosses, northern giant petrels and white-chinned petrels at South Georgia.
Discussion
Molecular and microscopy methods were used to screen for the presence of key blood parasites in a total of 269 birds from 5 species of albatrosses and 12 species of petrels sampled in the southwest Atlantic and Southern Ocean over a period of 11 years (2013–2023). None of the samples were found to be infected with parasites of the genera Plasmodium, Leucocytozoon, Haemoproteus, Borrelia, Anaplasma or Ehrlichia. Although detecting parasites in blood smears through microscopy is challenging when infection intensity is low (Valkiunas, Reference Valkiunas2005), the high sensitivity of molecular methods increases our confidence that none of the birds were infected. These results are consistent with other investigations of blood parasite infections conducted in seabirds of the Antarctic region (Laird, Reference Laird1961; Quillfeldt et al., Reference Quillfeldt, Martínez, Hennicke, Ludynia, Gladbach, Masello, Riou and Merino2010; Llanos et al., Reference Llanos, Suazo, Quillfeldt, Cursach and Salas2018). Screening of 455 birds from 14 species sampled between 1975 and 1978 in South Georgia found that none of the samples tested positive for blood parasites, except a small proportion of wandering, black-browed and grey-headed albatrosses, which were infected with the previously undescribed Hepatozoan albatrossi (Peirce and Prince, Reference Peirce and Prince1980). Documented cases of Hepatozoon in the Antarctic and subantarctic regions are limited to Hepatozoon albatrossi, reported in albatrosses and storm petrels (Merino et al., Reference Merino, Martínez, Masello, Bedolla and Quillfeldt2014; Parsons et al., Reference Parsons, Voogt, Schaefer, Peirce and Vanstreels2017). Our study aimed to screen for other parasites with poorly known occurrence, and excluded Hepatozoon because its presence is already established. Our findings provide further evidence that most seabird species are likely relatively free of blood parasites (Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011).
The lack of blood parasites in the samples may be explained partly by the harsh environmental conditions at the breeding grounds, which may preclude vector persistence (Martínez-Abraín et al., Reference Martínez-Abraín, Esparza and Oro2004). To date, there are no records of vectors such as hematophagous ceratopogonid or hippoboscid biting flies, or Aedes mosquitoes, in subantarctic or Antarctic islands where most of the study species nest (Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011; Ferreira et al., Reference Ferreira, Santiago-Alarcon, Braga, Santiago-Alarcon and Marzal2020). Such vectors may, however, occur in feeding areas, making disease transmission possible from infected coastal seabird or land bird species. Infection at non-breeding grounds is thought to drive the incidence of Leucocytozoon and Plasmodium lineages in Caspian gulls (Larus cachinnans) wintering on the coast of Poland (Zagalska-Neubauer and Bensch, Reference Zagalska-Neubauer and Bensch2016), and of Haemoproteus spp. in Manx shearwaters and black-browed albatrosses off the coast of Brazil (Sgarioni et al., Reference Sgarioni, Serafini, Pereira, Emmerich, Pontes, Machado, Ribeiro, Amorim, Klafke and Reck2024), since these species tested negative at their breeding colonies (Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011). The petrel and albatross species that were sampled in South Georgia, including white-chinned petrels, wandering albatrosses and northern giant petrels, can travel to the Patagonian Shelf or shelf-break to feed during the breeding season, and stay there for part or all of the nonbreeding season (Phillips et al., Reference Phillips, Silk, Croxall and Afanasyev2006; González‐Solís et al., Reference González‐Solís, Croxall and Afanasyev2007; Froy et al., Reference Froy, Lewis, Catry, Bishop, Forster, Fukuda, Higuchi, Phalan, Xavier, Nussey and Phillips2015; Clay et al., Reference Clay, Small, Tuck, Pardo, Carneiro, Wood, Croxall, Crossin and Phillips2019; Granroth-Wilding and Phillips, Reference Granroth-Wilding and Phillips2019). The lower latitudes of the Patagonian Shelf and shelf-break, compared to the Antarctic and sub-Antarctic regions, increase the likelihood of vector presence and infection risk, with the potential for subsequent transmission by returning migrants to colonies during the breeding season (Quillfeldt et al., Reference Quillfeldt, Arriero, Martínez, Masello and Merino2011; Sallaberry-Pincheira et al., Reference Sallaberry-Pincheira, Gonzalez-Acuña, Herrera-Tello, Dantas, Luna-Jorquera, Frere, Valdés-Velasquez, Simeone and Vianna2015). Indeed, haemosporidian parasites, such as P. relictum, P. circumflexum and P. vaughani, as well as Borrelia parasites, can be found in migratory birds (McDiarmid, Reference McDiarmid1969; Wolcott et al., Reference Wolcott, Margos, Fingerle and Becker2021; Bennett et al., Reference Bennett, Niebuhr, Lagrue, Middlemiss, Webster and Filion2024), and seabirds are thought to play a role in the dispersal of Anaplasma and Ehrlichia bacteria (Vanstreels et al., Reference Vanstreels, Yabsley, Parsons, Swanepoel and Pistorius2018; Muñoz-Leal et al., Reference Muñoz-Leal, Clemes, Lopes, Acosta, Serpa, Mayorga, Gennari, González-Acuña and Labruna2019). As such, the routine surveillance for blood parasite infections in seabirds in the southwest Atlantic and Southern Ocean is essential for detecting any shifts of disease vectors to higher latitudes, thereby increasing risks of range expansions for vector-borne parasites.
While the lack of detectable blood parasites is reassuring, seabirds of the southwest Atlantic and Southern Ocean remain at risk of future infections. Ehrlichia spp. was recorded recently in southern Chile in an I. uriae tick (Muñoz-Leal et al., Reference Muñoz-Leal, Clemes, Lopes, Acosta, Serpa, Mayorga, Gennari, González-Acuña and Labruna2019), which is a common parasite of seabirds on Antarctic and subantarctic islands (Vanstreels et al., Reference Vanstreels, Palma and Mironov2020), and new Plasmodium infections were recently recorded in seabirds in New Zealand, including in a procellariiform species, the Westland petrel (Procellaria westlandica) (Bennett et al., Reference Bennett, Niebuhr, Lagrue, Middlemiss, Webster and Filion2024). Many albatrosses and petrels already face numerous other threats, so novel infections are potentially serious additional risks (Heard et al., Reference Heard, Smith, Ripp, Berger, Chen, Dittmeier, Goter, Mcgarvey and Ryan2013; Dias et al., Reference Dias, Martin, Pearmain, Burfield, Small, Phillips, Yates, Lascelles, Borborolu and Croxall2019; Phillips et al., Reference Phillips, Fort, Dias, Young and VanderWerf2023). As a result, developing conservation and management plans for seabirds of the southwest Atlantic and Southern Ocean will require the implementation of proactive risk assessments, biosecurity measures and long-term disease surveillance, particularly at important breeding and non-breeding areas (Uhart et al., Reference Uhart, Gallo and Quintana2018). We recommend that surveillance programmes of blood parasite infections go beyond relying only on visual observations of diseased birds, and incorporate active screenings of seabird samples.
Supplementary material
The supplementary material for this article can be found at https://doi.org/10.1017/S0031182025100590.
Acknowledgements
We are very grateful to the field assistants who helped with the sampling at Bird Island. The authors are also grateful to all teams and volunteers dedicated to work with monitoring sick and dead seabirds stranded along the Brazilian coast as part of the Beach Monitoring Project of Petrobras, as well as for all teams engaged providing samples and data for the biobank ‘Banco Nacional de Amostras Biologicas de Albatrozes e Petreis’ (BAAP), which holds samples of birds bycaught in Brazilian fisheries and from seabirds stranding networks in Brazil.
Author contributions
P.P.S., A.Z.S., C.B. and R.A.P. conceptualized the study. R.A.P., A.P., P.P.S., T.E., T.P.P., D.B.A., C.M.K., A.C.D.B. and K.H.L. were responsible for samples and data curation. P.P.S. and A.Z.S. conducted laboratory screening and diagnosis. P.P.S. conducted the literature searches, performed formal analysis and wrote the original draft of the manuscript. R.A.P., A.O.S.L., G.K., J.R., A.C.D.B., K.H.L. and C.B. were responsible for validation, supervision and final review & editing. All authors revised and edited the manuscript providing input for the manuscript structure and topics. P.P.S. and A.Z.S. constructed the table and graphical abstract.
Financial support
This work represents a contribution to the Ecosystems component of the British Antarctic Survey Polar Science for a Sustainable Planet Programme, funded by the Natural Environment Research Council. Part of this work was carried out during a secondment funded by the Agreement on the Conservation of Albatrosses and Petrels. The studied birds were mainly collected and necropsied as part of the Beach Monitoring Project of the Santos Basin (Projeto de Monitoramento de Praias – PMP/BS). PMP is one of the monitoring programs required by Brazil’s federal environmental agency, the Institute of the Environment and Renewable Natural Resources (IBAMA), for the environmental licensing process of oil production and transport by Petrobras. Bainy and K.H. Lüchmann are recipients of a productivity fellowship from CNPq (311725/2021-0 and 313843/2023-6, respectively). We are thankful to CEMAVE/ICMBio, Petrobras, IBAMA, LABCAI/UFSC and R3 Animal for their continued support, and the Wildlife Conservation Network for providing a veterinary scholarship to A. Z. Sgarioni.
Competing interests
The authors declare there are no conflicts of interest.
Ethical standards
Sampling of live birds at Bird Island was approved by the British Antarctic Survey Animal Welfare and Ethics Committee and carried out with the permission of the Government of South Georgia and the South Sandwich Islands. Sampling from stranded and deceased seabirds in this project was undertaken with all the necessary permits issued by SISBIO/ICMBio and IBAMA, environmental agencies of Brazil.
Open access
