Terns are a highly migratory group of seabirds that are found worldwide. In Ireland, there are five species of commonly breeding tern: Little Tern Sternula albifrons, Roseate Tern Sterna dougallii, Arctic Tern S. paradisaea, Common Tern S. hirundo and Sandwich Tern S. sandvicensis. Prior work has demonstrated that whilst many Irish tern species, including Common and Roseate Terns, are increasing in abundance, the productivity of these species can be low. Multiple factors may influence the ability of adult terns to successfully raise chicks, including food availability, provisioning rates, colony density, dependence effects, and/or disease. Here, we investigated factors contributing to the mortality of young terns from Rockabill Island in the Republic of Ireland, which supports the largest breeding population of Roseate Terns in Europe. To better understand the factors contributing to the deaths of young birds, we analysed the macroscopic and microscopic characteristics of necropsies of 60 young Common, Arctic and Roseate Terns. Of the carcasses that we examined, 41 showed congested blood circulation in the lungs and head simultaneously, and of the remaining 19 birds, only five presented a clear cause of death. Here, we outline descriptions of these carcasses in addition to recommendations of further investigations that might help to confirm the causal factors leading to young tern mortality.

Their marine specialisation, predatory roles and long lifespans mean that seabirds, including terns, are sensitive to changes in the marine environment (Dunn 2019) and are considered marine sentinels (Thibault et al. 2019). Changes in seabird population health and breeding success may therefore denote negative impacts deriving from pollution, food availability, or shifts in climate patterns (Furness & Camphuysen 1997). Seabirds are often directly exposed to anthropogenic impacts in the marine environment, including chemical substances (Pacyna et al. 2019), overfishing (Dias et al. 2019) and plastic pollution (Cartraud et al. 2019). Seabirds become contaminated via their diets, due to their predatory roles (Cairns 1988), and can then accumulate substances, such as pollutants, within their tissues. Seabirds therefore function as indicators of ecosystem health in marine environments (Cairns 1988).

Due to their wide-ranging nature, seabirds can act as vectors for the transmission of pathogens (bacteria, viruses and fungi) and parasites across both terrestrial and marine habitats (Mallory et al. 2010). Indeed, the life history characteristics of seabirds, such as their longevity, migratory behaviour, and affinity to densely packed breeding colonies, likely aid the transfer of infectious agents between both individuals and colonies (Schreiber & Burger 2001). For example, studies examining external parasites (i.e. ticks) in seabirds have shown evidence of trans-oceanic host dispersal of tick-borne pathogens like the zoonotic intracellular bacterium Coxiella sp. (Dietrich et al. 2011; Gómez-Díaz et al. 2012; Duron et al. 2014; McCoy et al. 2016). While parasites are recognised as important components of marine ecosystems (McCoy et al. 2016; Khan et al. 2019), both external (e.g. ticks and mites) and internal (e.g. cestodes, nematodes and trematodes) parasites can affect their seabird host via competition for resources (Khan et al. 2019). For example, tick infestations have led to increased mortality in both Black-browed Albatross Thalassarche melanophris and Roseate Tern Sterna dougallii colonies (Bergström et al. 1999; Ramos et al. 2001). Furthermore, internal parasites are common in seabirds, and both adult and juvenile birds are exposed to a variety of intestinal parasites via their food consumption (Gaspard & Schwartzbrod 2003).

In addition to parasites, a range of pathogens also infect seabirds. One example of this is ‘the Tern virus’, a virus described in Common Terns S. hirundo in South Africa after a mass mortality event in 1961, which bears similarities to Newcastle disease (Alexander 1995). The Tern virus belongs to the myxovirus group and was classified as Influenza A H5N3, via identification from bird carcasses stranded on beaches in Capetown, South Africa (Rowan 1962; Becker 1963; Becker 1966). Avian Influenza A viruses are considered a global public health threat because they are zoonotic (transmission from animals to humans is possible) and can be fatal to humans (Perdue & Swayne 2005). Indeed, many viral pathogens are highly mutatable, and can adapt quickly and infect a wide range of hosts (Amitai et al. 2020). Another influenza strain, Influenza A H5N1, originated in domestic animals and evolved to spread worldwide, infecting different hosts, including wild birds and humans (Perkins & Swayne 2002). Due to the potential wide-spread impacts of parasites and pathogens, monitoring of bird colonies is an important part of disease surveillance (Parson & Vanstreels 2016), not solely for conserving bird colonies, but also for having the potential to protect the health of livestock and humans (Brunner et al. 2009).

When faced with infection via parasitism and/or pathogens, seabirds have evolved a range of defence mechanisms. Initially, the innate immune system, involving maternal antibodies, protects chicks during the first weeks of life and includes phagocytic cells, complement serum proteins (which work together with antibodies to lyse target cells), and other blood proteins, all of which help to create both chemical and physical barriers (Hammouda et al. 2012). In addition, the adaptive immune system (B and T cells, humoral immunity) is important for defending against some specific pathogen infections and is developed through host exposure to a pathogen (Rumińska et al. 2008). The primary organs involved in the development of adaptive immunity in birds are the bursa of Fabricius, the thymus and bone marrow (Davison et al. 2008). However, other lymphoid organs, such as the spleen, the mucosa associated with lymphoid tissue, and more diffuse lymphoid tissues, are secondary sites of blood cell production that contribute to immunity (Davison 2014). Because younger birds are less likely to have prior exposure to infections, they may be more susceptible to diseases than adults (Härtle et al. 2013). Chicks that survive this initial period will go on to develop adaptive immunity from pathogen exposure, helping to defend themselves against future infections (Pihlaja et al. 2006).

Here we studied young Common, Arctic S. paradisaea, and Roseate Terns from Rockabill Island, off the east coast of the Republic of Ireland (53°35’N 6°00’W). These terns inhabit Irish waters during the breeding season months of late April to September, before migrating to western and southern Africa during the post- breeding period (Seward et al. 2019). All three species are considered of ‘Least Concern’ according to the International Union for the Conservation of Nature Red List (IUCN 2018), due to the implementation of conservation efforts over recent decades (Cabot 1996; Hoffmann et al. 1996; Amaral et al. 2010). Indeed, Roseate and Common Tern populations in Britain and Ireland have increased since the 1980s and the start of species-focused conservation projects (Lloyd et al. 2010). However, more recently, these tern species have been ‘Amber-listed’ and are of ‘medium conservation concern’ in Ireland, according to the recent Birds of Conservation Concern in Ireland (BoCCI) review (Gilbert et al. 2021). Furthermore, within Britain, Roseate Terns have been assigned to the UK ‘Red List’ and are of ‘high conservation concern’ within the most recent Birds of Conservation Concern in the United Kingdom, Channel Islands and Isle of Man assessment (Stanbury et al. 2021). Factors likely to influence tern population trends include predation by invasive American Mink Neovison vison, Red Fox Vulpes vulpes, Herring Gull Larus argentatus and Common Kestrels Falco tinnunculuset al.i>, reduced availability of important prey fish (e.g. sandeels), and trapping in their African wintering grounds (Mitchell et al. 2004; Sugoto et al. 2009). Conservation efforts are ongoing in Ireland, and Rockabill Island was recently managed as part of an EU LIFE Nature- funded Roseate Tern Project (2015–22).

Here, we examined fresh carcasses of Common, Roseate and Arctic Terns that were recovered daily during the 2018 breeding season on Rockabill Island. We describe both the macroscopic findings from necropsies and the microscopic findings from histological examinations. In particular, we present a health assessment of young terns from Rockabill Island, thereby focusing on a relatively understudied life history stage.

The authors wish to thank BirdWatch Ireland, the Rockabill Island wardens (Luíse Ní Dhonnabháin & David Miley), and boat crew for their support in collecting samples; laboratory technicians, Mary Veldon and John Kennedy, at the Atlantic Technological University for their support; and anonymous reviewers for their comments.

Abdo-El-Shamy, S. 2012. Bioaccumulation of some heavy metals and histopathological, ultrastructure alternation in kidney, brain and lung of migratory birds around Manzala Lake. Assiut Veterinary Medicine Journal 58: 134. [Crossref]

Acampora, H., White, P., Lyashevska, O. & O’Connor, I. 2017. Presence of persistent organic pollutants in a breeding common tern (Sterna hirundo) population in Ireland. Environmental Science and Pollution Research 24: 13025–13035. [Crossref]

Alexander, D. J. 1995. The epidemiology and control of avian influenza and Newcastle disease. Journal of Comparative Pathology 112:105–126. [Crossref]

Alexander, D. J. 2000. A review of avian influenza in different bird species. Veterinary Microbiology 74: 3–13. [Crossref]

Amaral, J. J., Almeida, S., Sequeira, M. & Neves, V. C. 2010. Black rat Rattus rattus eradication by trapping allows recovery of breeding roseate tern Sterna dougallii and common tern S. hirundo populations on Feno Islet, the Azores, Portugal. Conservation Evidence 7: 16–20.

Amitai, A., Sangesland, M., Lingwood, D. & Chakraborty, A. 2020. Influenza virus geometry shapes the immune response against it. Bulletin of the American Physical Society 65: 1–10.

Baird, P. H. 1990. Influence of abiotic factors and prey distribution on diet and reproductive success of three seabird species in Alaska. Ornis Scandinavica 21: 224–235. [Crossref]

Baldwin, S. P., Oberholser, H. C. & Worley, L. G. 1931. Measurements of birds, Cleveland Museum of Natural History: 1–167. Cleveland Museum of Natural History, Ohio. [Crossref]

Balog, J. M. 2003. Ascites syndrome (pulmonary hypertension syndrome) in broiler chickens: Are we seeing the light at the end of the tunnel? Avian and Poultry Biology Reviews 14: 99–126. [Crossref]

Bancroft, J. D. & Gamble, M. 2012. Theory and Practice of Histological Techniques, 6th Edition: 1–699. Churchill Livingstone, Edinburgh.

Becker, P. H. & Finck, P. 1986. The meaning of nest density and nest location for the breeding success of Common Tern Sterna hirundo in colonies of a Wadden Sea island. Ornithological Institute 33: 192–207.

Becker, W. B. 1963. The morphology of tern virus. Virology 20: 318–27. [Crossref]

Becker, W. B. 1966. The isolation and classification of tern virus: influenza virus A/tern/South Africa/1961. Journal of Hygiene 64: 309–320. [Crossref]

Benskin, C. M. H., Wilson, K., Jones, K. & Hartley, I. R. 2009. Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biological Reviews 84: 349–373. [Crossref]

Bergström, S., Haemig, P. D. & Olsen, B. 1999. Increased mortality of black-browed albatross chicks at a colony heavily-infested with the tick Ixodes uriae. International Journal for Parasitology 29: 1359–1361. [Crossref]

Bouwhuis, S., Vedder, O. & Becker, P. H. 2015. Sex-specific pathways of parental age effects on offspring lifetime reproductive success in a long-lived seabird. Evolution 69: 1760–1771. [Crossref]

Brunner, E. J., Jones, P. J., Friel, S. & Bartley, M. 2009. Fish, human health and marine ecosystem health: policies in collision. International Journal of Epidemiology 38: 93–100. [Crossref]

Burger, J. & Gochfeld, M. 2001. Effects of chemicals and pollution on seabirds. In: Schreiber, E. A. & Burger, J. Biology of Marine Birds: 485–525. CRC Press, Florida. [Crossref]

Cabot, D. 1996. Performance of the Roseate Tern Population Breeding in North-West Europe: Ireland, Britain and France, 1960–94. Biology and Environment: Proceedings of the Royal Irish Academy 96B: 55–68.

Cairns, D. K. 1988. Seabirds as indicators of marine food supplies. Biological Oceanography 5: 261–271.

Camphuysen, C. J. & Garthe, S. 2000. Seabirds and commercial fisheries: population trends of piscivorous seabirds explained? In: Kaiser M. J. & de Groot S. J. (eds.) The effects of fishing on non-target species and habitats: Biological, conservation and socio-economic issues: 163–184. Blackwell, New Jersey.

Cartraud, A. E., Le Corre, M., Turquet, J. & Tourmetz, J. 2019. Plastic ingestion in seabirds of the western Indian Ocean. Marine Pollution Bulletin 140: 308–314. [Crossref]

Cook, A. S. C. P., Dadam, D., Mitchell, I., Ross-Smith, V. H. & Robinson, R. A. 2014. Indicators of seabird reproductive performance demonstrate the impact of commercial fisheries on seabird populations in the North Sea. Ecological Indicators 38: 1–11. [Crossref]

Cummins, S., Lewis, L. J. & Egan, S. 2016. Life on the Edge – Seabirds and Fisheries in Irish Waters. BirdWatch Ireland Report: 43.

Davison, F. 2014. The importance of the avian immune system and its unique features. In: Schat, K. A., Kaspers, B. & Kaiser, P. Avian Immunology, 2nd Edition: 1–9. Academic Press, London. [Crossref]

Davison, F., Kaspers, B. & Schat, K. A. 2008. The Avian Mucosal Immune System. In: Davison, F., Kaspers, B. & Schat, K. A. Avian Immunology, 1st Edition: 241–242. Academic Press, London. [Crossref]

Deschutter, A. & Lesson, S. 1986. Feather growth and development. World's Poultry Science Journal 42: 259–267.

Dias, M. P., Martin, R., Pearmain, E. J., Burfield, I. J., Small, C., Phillips, R. A., Yates, O., Lascelles, B. Borboroglu, G. P. & Croxall, J. P. 2019. Threats to seabirds: a globalassessment. Biological Conservation 237: 525–537. [Crossref]

Diaz, L. A., Komar, N., Visintin, A., Juri, M. J. D., Stein, M., Allende, R. L., Spinsanti, L., Konigheim, B., Aguilar, J., Laurito, M., Almirón, W. & Contigiani M. 2008. West Nile virus in birds, Argentina. Emerging Infectious Diseases 14: 689. [Crossref]

Dietrich, M., Gómez-Díaz, E. & McCoy, K. D. 2011. Worldwide distribution and diversity of seabird ticks: implications for the ecology and epidemiology of tick-borne pathogens. Vector-Borne and Zoonotic Diseases 11: 453–470. [Crossref]

Donadieu, E., Bahuon, C., Lowenski, S., Zientara, S., Coulpier, M. & Lecollinet, S. 2013. Differential virulence and pathogenesis of West Nile viruses. Viruses 5: 2856–2880. [Crossref]

Dunn, P. O. 2019. Changes in timing of breeding and reproductive success in birds. Effects of Climate Change on Birds 9: 113–128. [Crossref]

Duron, O., Jourdain, E. & McCoy, K. D. 2014. Diversity and global distribution of the Coxiella intracellular bacterium in seabird ticks. Ticks and Tick-borne Diseases 5: 557–563. [Crossref]

Elkin, N. 2019. Poultrymed: Atlases: Histopathology: Avian encephalomyelitis. (www.poultrymed.com/Poultrymed/Templates/showpage.asp?DBID=1&LNGID=1&TMID=103&FID=1607). Accessed April 2022.

Forster, P. 2014. Ten years on: Generating innovative responses to avian influenza. Ecohealth 11: 15–21. [Crossref]

Furness, R. W. & Camphuysen, K., 1997. Seabirds as monitors of the marine environment. ICES Journal of Marine Science 54: 726–737. [Crossref]

Gaspard, P. G. & Schwartzbrod, J. 2003. Parasite contamination (helminth eggs) in sludge treatment plants: definition of a sampling strategy. International Journal of Hygiene and Environmental Health 206: 117–122. [Crossref]

Gaston, A. J., Chapdelaine, G. & Noble, D. G. 1983. The growth of Thick-billed Murre chicks at colonies in Hudson Strait: inter-and intra-colony variation. Canadian Journal of Zoology 61: 2465–2475. [Crossref]

Gilbert, G., Stanbury, A. & Lewis, L. 2021. Birds of conservation concern in Ireland 4: 2020–2026. Irish Birds 43: 1–22.

Gómez-Díaz, E., Morris-Pocock, J. A., González-Solís, J. & McCoy, K. D. 2012. Trans-oceanic host dispersal explains high seabird tick diversity on Cape Verde islands. Biology Letters 8: 616–619. [Crossref]

Grace-Jones, W. 2012. Tissue Microarray. In: Bancroft, D. & Gamble, M. (eds.) Theory and Practice of Histological Techniques, 6th Edition: 527–535. Churchill Livingstone, Edinburgh. [Crossref]

Hammouda, A., Selmi, S., Pearce-Duvet, J., Chokri, M. A., Arnal, A., Gauthier-Clerc, M. & Boulinier, T. 2012. Maternal Antibody Transmission in Relation to Mother Fluctuating Asymmetry in a Long-Lived Colonial Seabird: The Yellow-Legged Gull Larus michahellis. PLOS ONE 7: e34966. [Crossref]

Harris, M. P., Newell, M., Daunt, F., Speakman, J. R. & Wanless, S. 2008. Snake Pipefish Entelurus aequoreus are poor food for seabirds. Ibis 150: 413–415. [Crossref]

Härtle S., Magor K. E., Göbel, T. W., Davison, F. & Kaspers, B. 2013. Structure And Evolution of Avian Immunoglobulins. In: Schat K. A., Kaspers B. & Kaiser P. Avian Immunology, 2nd Edition: 103–120. Academic Press, London. [Crossref]

Hoffman, D. J., Ohlendorf, H. M. & Aldrich, T. W. 1988. Selenium teratogenesis in natural populations of aquatic birds in central California. Archives of Environmental Contamination and Toxicology 17: 519–525. [Crossref]

Hoffmann, L., Hafner, H. & Salathé, T. 1996. The contribution of colonial waterbird research to wetland conservation in the Mediterranean region. Colonial Waterbirds 19: 12–30. [Crossref]

Horimoto, T. & Kawaoka, Y. 2001. Pandemic threat posed by avian influenza A virus. Clinical Microbiology Reviews 14: 129–149. [Crossref]

Hubálek, Z. 2004. An annotated checklist of pathogenic microorganisms associated with migratory birds. Journal of Wildlife Diseases 40: 639–659. [Crossref]

Hunt Jr, G. L., Eppley, Z. A. & Schneider, D. C. 1986. Reproductive performance of seabirds: the importance of population and colony size. The Auk 103: 306–317. [Crossref]

IUCN 2018. The IUCN Red List of the Threatened Species. Version 2018-2019. (www.iucnredlist.org). International Union for Conservation of Nature. Accessed January 2019.

Jindal, N., Mahajan, N. K., Mittal, D., Gupta, S. L. & Khokhar, R. S. 2004. Some epidemiological studies on infectious bursal disease in broiler chickens in parts of Haryana,India. International Journal of Poultry Science 3: 478–482. [Crossref]

JNCC 2021. Common tern (Sterna hirundo). (jncc.gov.uk/our-work/common-tern-sterna-hirundo). Joint Nature Conservation Committee. Accessed April 2022.

Jones, Y. L. & Swayne, D. E. 2004. Comparative pathobiology of low and high pathogenicity H7N3 Chilean avian influenza viruses in chickens. Avian Diseases 48: 119–128. [Crossref]

Julian, R. J. 1993. Ascites in poultry. Avian Pathology 22: 419–454. [Crossref]

Kamiński, M., Janiszewski, T., Indykiewicz, P., Nowakowski, J. J., Kowalski, J., Dulisz, B. & Minias, P. 2021. Density-dependence of nestling immune function and physiological condition in semi-precocial colonial bird: a cross-fostering experiment. Frontiers in Zoology 18: 7. [Crossref]

Keawcharoen, J., van Riel, D., van Amerongen, G., Bestebroer, T., Beyer, W. E., van Lavieren, R., Osterhaus, A. D. M. E., Fouchier, R. A. M. & Kuiken, T. 2008. Wild ducks as long-distance vectors of highly pathogenic avian influenza virus (H5N1). Emerging Infectious Diseases 14: 600. [Crossref]

Khan, J. S., Provencher, J. F., Forbes, M. R., Mallory, M. L., Lebarbenchon, C. & McCoy, K. D. 2019. Parasites of seabirds: A survey of effects and ecological implications. Advances in Marine Biology 82: 1–50. [Crossref]

Kim, H. R., Kwon,Y. K., Jang, I., Lee,Y. J., Kang, H. M., Lee, E. K. & Lee, H. K. 2015. Pathologic changes in wild birds infected with highly pathogenic avian influenza A (H5N8) viruses, South Korea, 2014. Emerging Infectious Diseases 21: 775. [Crossref]

Koratkar, S. S., Pawar, S. D., Shelke, V. N., Kale, S. D. & Mishra, A. C. 2014. Pathogenicity of avian influenza H11N1 virus isolated from wild aquatic bird Eurasian Spoonbill (Platalea leucorodia). The Indian Journal of Medical Research 139: 782.

Kozdrun W., Czekaj H. & Stys N. 2015. Avian zoonoses – a review. Bulletin of the Veterinary Institute in Pulawy 59: 171–178. [Crossref]

Lean, F. Z., Núñez, A., Banyard, A. C., Reid, S. M., Brown, I. H. & Hansen, R. D. 2021. Gross pathology associated with highly pathogenic avian influenza H5N8 and H5N1 in naturally infected birds in the UK (2020–2021). Veterinary Record 190: e731. [Crossref]

Lewis, S., Sherratt, T. N., Hamer, K. C. & Wanless, S. 2001. Evidence of intra-specific competition for food in a pelagic seabird. Nature 412: 816–819.

Liu, J., Xiao, H., Lei, F., Zhu, Q., Qin, K., Zhang, X. W., Zhang, L. X., Zhao, D, Whang, G., Feng, Y., Ma, J., Liu, W., Wang, J. & Gao, F. 2005. Highly pathogenic H5N1 influenza virus infection in migratory birds. Science 309: 1206–1206. [Crossref]

Lloyd, C., Tasker, M. L. & Partridge, K. (eds.) 2010. The Status of Seabirds in Britain and Ireland. Poyser, London.

Mallory, M. L., Robinson, S. A., Hebert, C. E. & Forbes, M. R. 2010. Seabirds as indicators of aquatic ecosystem conditions: a case for gathering multiple proxies of seabird health. Marine Pollution Bulletin 60: 7–12. [Crossref]

de Matos, A. M. R. N., Domit, C. & Bracarense, A. P. F. R. L. 2020. Seabirds: studies with parasitofauna and potential indicator for environmental anthropogenic impacts. Semina: Ciências Agrárias 41: 1439–1450. [Crossref]

Marusak, R. A., Guy, J. S., Abdul-Azis, T. A., West, M. A., Fletcher, O. J., Day, J. M., Zsak, L. & Barner, J. H. 2010. Parvovirus-associated cerebellar hypoplasia and hydrocephalus in day old broiler chickens. Avian Diseases 54: 156–160. [Crossref]

Massias A. & Becker P. H. 1990. Nutritive value of food and growth in Common Tern Sterna hirundo chicks. Ornis Scandinavica 21: 187–194 [Crossref]

McCoy, K. D., Dietrich, M., Jaeger, A., Wilkinson, D. A., Bastien, M., Lagadec, E., Boulinier, T., Pascalis, H., Tortosa, P., Le Corre, M., Dellagi, K. & Lebarbenchon, C. 2016. The role of seabirds of the Iles Eparses as reservoirs and disseminators of parasites and pathogens. Acta Oecologica 72: 98–109. [Crossref]

McKnight, A., Blomberg, E. J., Irons, D. B., Loftin, C. S. & McKinney, S. T. 2019. Survival and recruitment dynamics of Black-legged Kittiwakes Rissa tridactyla at an Alaskan colony. Marine Ornithology 47: 209–222.

Minias, P., Gach, K., Włodarczyk, R. & Janiszewski, T. 2019. Colony size affects nestling immune function: a cross-fostering experiment in a colonial waterbird. Oecologia 190: 333–341. [Crossref]

Mitchell, I. Daunt, F., Frederiksen, M. & Wade, K. 2020. Impacts of climate change on seabirds, relevant to the coastal and marine environment around the UK. MCCIP Science Review 2020: 382–399.

Mitchell, P. I., Newton, S. F., Ratcliffe, N. & Dunn, T. E. (eds.) 2004. Seabird populations of Britain and Ireland: Results of the Seabird 2000 census (1998–2002). Poyser, London.

Mohamed, M. H. 2013. Pathology of Poultry Diseases, lesions of avian diseases.(issuu.com/mohamedelariny/docs/poultry_diseases2). Accessed April 2022.

Monaghan, P. 1992. Seabirds and sandeels: the conflict between exploitation and conservation in the northern North Sea. Biodiversity & Conservation 1: 98–111. [Crossref]

Nur, N. 1988. The cost of reproduction in birds: an examination of the evidence. Ardea 55: 155–168. [Crossref]

Pacyna, A. D., Jakubas, D., Ausems, A. N., Frankowski, M., Polkowska, Ż. & Wojczulanis-Jakubas, K. 2019. Storm petrels as indicators of pelagic seabird exposure to chemical elements in the Antarctic marine ecosystem. Science of the Total Environment 692: 382–392. [Crossref]

Padilla L. R., Whiteman, N. K., Merkel, J., Huyvaert, K. & Parker P. G. 2006. Health assessment of seabirds on Isla Genovesa, Galapagos Islands. Ornithological Monographs 6: 86–97. [Crossref]

Parson, N. J. & Vanstreels, R. E. T. V. 2016. Southern African Seabird Colony Diseases Risk assessment: 1–53. Southern African Foundation for the Conservation of Coastal Birds, Cape Town.

Perdue, M. L. & Swayne, D. E. 2005. Public health risk from avian influenza viruses.Avian Diseases 49: 317–327. [Crossref]

Perkins, L. E. & Swayne, D. E. 2001. Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Veterinary Pathology 38: 149–164. [Crossref]

Perkins, L. E. L. & Swayne, D. E. 2002. Susceptibility of laughing gulls (Larus atricilla) to H5N1 and H5N3 highly pathogenic avian influenza viruses. Avian Diseases 46: 877–885. [Crossref]

Piec, D. & Dunn, E. K. 2021. International (East Atlantic) Species Action Plan for the Conservation of the Roseate Tern Sterna dougallii (2021–2030): 1–60. European Commission 2021.

Pihlaja, M., Siitari, H. & Alatalo, R. V. 2006. Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. Journal of Animal Ecology 75: 1154–1164. [Crossref]

Power, A., White, P., McHugh, B., Berrow, S., Schlingermann, M., McKeown, A., Cabot, D., Tannian, M., Newton, S., McGovern, E., Murphy, S., Crowley, D., O'Hea, L., Boyle, B. & O’Connor, I. 2021. Persistent pollutants in fresh and abandoned eggs of Common Tern (Sterna hirundo) and Arctic Tern (Sterna paradisaea) in Ireland. Marine Pollution Bulletin 168: 112400. [Crossref]

R Core Team 2020. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org.

Rae, M. A. 2006. The diagnostic value of necropsy. In: Harrison, G. J. & Lightfoot, T. L. (eds.). Clinical Avian Medicine, 2nd Edition: 661–678. Spix Publishing, Florida

Ramos, J. A., Bowler, J., Davis, L., Venis, S., Quinn, J. & Middleton, C. 2001. Activity patterns and effect of ticks on growth and survival of tropical Roseate Tern nestlings. The Auk 118: 709–716. [Crossref]

Reynolds, D. L. 1998. JOURMethod to Provide Artificial Passive Immunity in BirdsNAL , Iowa State University Research Foundation, Inc., Ames, Iowa, U.S. Patent and Trademark Office, Patent number 5,807,551.

Roman, L., Kastury, F., Petit, S., Aleman, R., Wilcox, C., Hardesty, B. D. & Hindell, M. A. 2020 Plastic, nutrition and pollution; relationships between ingested plastic and metal concentrations in the livers of two Pachyptila seabirds. Scientific Reports 10: 1–14. [Crossref]

Rowan, M. K. 1962. Mass mortality among European Common terns in South Africa in April– May 1961. British Birds 55: 103–114.

Rumińska, E., Koncicki, A. & Stenzel, T. 2008. Structure and function of the avian immune system in birds. Medycyna Weterynaryjna 64: 265–268.

Rutkowska, M., Bajger-Nowak, G., Kowalewska, D., Bzoma, S., Kalisińska, E., Namieśnik, J. & Konieczka, P. 2019. Methylmercury and total mercury content in soft tissues of two bird species wintering in the Baltic Sea near Gdansk, Poland. Chemosphere 219: 140–147. [Crossref]

Schreiber, E. A. & Burger, J. 2001. Seabirds In the Marine Environment. In: Schreiber, E. A. & Burger, J. (eds.), Biology of Marine Birds, 1–15. CRC Press, Florida. [Crossref]

Schrimpf, M. B., Parrish, J. K. & Pearson, S. F. 2012. Trade-offs in prey quality and quantity revealed through the behavioral compensation of breeding seabirds. Marine Ecology Progress Series 460: 247–259. [Crossref]

Seward, A., Ratcliffe, N., Newton, S., Caldow, R., Piec, D., Morrison, P., Cadwallender, T, Davies, W. & Bolton, M. 2019. Metapopulation dynamics of roseate terns: Sources, sinks and implications for conservation management decisions. Journal of Animal Ecology 88: 138–153. [Crossref]

Slaoui, M. & Fiette, L. 2011. Histopathology procedures: from tissue sampling to histopathological evaluation. In: Gautier, J. C. (eds) Drug Safety Evaluation: Methods and Protocols: 69–82. Humana Press, New York. [Crossref]

Stallknecht, D. E., Nagy, E., Hunter, D. B. & Slemons, R. D. 2007. In Avian influenza. In: Thomas, N. J., Hunter, D. B. & Atksinson, C. T. (eds.) Infectious diseases of wild birds: 108– 130. Blackwell Press, Oxford. [Crossref]

Stanbury, A., Eaton, M., Aebischer, N., Balmer, D., Brown, A., Douse, A., Lindley, P., McCulloch, N., Noble, D. & Win, I. 2021. The status of our bird populations: the fifth Birds of Conservation Concern in the United Kingdom, Channel Islands and Isle of Man and second IUCN Red List assessment of extinction risk for Great Britain. British Birds 114: 723–747.

Suddaby, D. & Ratcliffe, N. 1997. The effects of fluctuating food availability on breeding Arctic Terns (Sterna paradisaea). The Auk 114: 524–530. [Crossref]

Sugoto. R., Reid, N. & McDonald, R. A. 2009. A Review of Mink Predation and Control for Ireland. Irish Wildlife Manuals 40: 1–61.

Taubenberger, J. K. & Morens, D. M. 2008. The pathology of influenza virus infections. Annual Review of Pathology: Mechanisms of Disease 3: 499–522. [Crossref]

Tella, J. L., Forero, M. G., Bertellotti, M., Donázar, J. A., Blanco, G. & Ceballos, O. 2001.Offspring body condition and immunocompetence are negatively affected by high breeding densities in a colonial seabird: a multiscale approach. Proceedings of the Royal Society of London. Series B: Biological Sciences 268: 1455–1461. [Crossref]

Thibault, M., Houlbreque, F., Lorrain, A. & Vidal, E. 2019. Seabirds: Sentinels beyond the oceans. Science 366: 813. [Crossref]

Vanezis, P. 2001. Interpreting bruises at necropsy. Journal of Clinical Pathology 54: 348–355. [Crossref]

Wendeln, H. & Becker, P. H. 1999.Effects of parental quality and effort on the reproduction of Common terns. Journal of Animal Ecology 68: 205–214. [Crossref]

White, S. J. & Kehoe, C. V. 2001. Difficulties in determining the age of Common Terns in the field. British Birds 94: 268–277.