An investigation into factors contributing to mortality of young terns at a managed colony
* Correspondence author. Email: firstname.lastname@example.org
1 Marine and Freshwater Research Centre, Atlantic Technological University, Old Dublin Road, Galway, H91 T8NW, Ireland;
2BirdWatch Ireland, Unit 20, Block D, Bullford Business Campus, Kilcoole, Co. Wicklow, A63 RW83, Ireland.
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.
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.
Influenza virus geometry shapes the immune response against it. Bulletin of the American Physical Society 65: 1–10.
Theory and Practice of Histological Techniques, 6th Edition: 1–699. Churchill Livingstone, Edinburgh.
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.
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.
Seabirds as indicators of marine food supplies. Biological Oceanography 5: 261–271.
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.
Life on the Edge – Seabirds and Fisheries in Irish Waters. BirdWatch Ireland Report: 43.
Feather growth and development. World's Poultry Science Journal 42: 259–267.
www.poultrymed.com/Poultrymed/Templates/showpage.asp?DBID=1&LNGID=1&TMID=103&FID=1607). Accessed April 2022.Poultrymed: Atlases: Histopathology: Avian encephalomyelitis. (
Birds of conservation concern in Ireland 4: 2020–2026. Irish Birds 43: 1–22.
www.iucnredlist.org). International Union for Conservation of Nature. Accessed January 2019.The IUCN Red List of the Threatened Species. Version 2018-2019. (
jncc.gov.uk/our-work/common-tern-sterna-hirundo). Joint Nature Conservation Committee. Accessed April 2022.Common tern (Sterna hirundo). (
Pathogenicity of avian influenza H11N1 virus isolated from wild aquatic bird Eurasian Spoonbill (Platalea leucorodia). The Indian Journal of Medical Research 139: 782.
Evidence of intra-specific competition for food in a pelagic seabird. Nature 412: 816–819.
The Status of Seabirds in Britain and Ireland. Poyser, London.
Survival and recruitment dynamics of Black-legged Kittiwakes Rissa tridactyla at an Alaskan colony. Marine Ornithology 47: 209–222.
Impacts of climate change on seabirds, relevant to the coastal and marine environment around the UK. MCCIP Science Review 2020: 382–399.
Seabird populations of Britain and Ireland: Results of the Seabird 2000 census (1998–2002). Poyser, London.
issuu.com/mohamedelariny/docs/poultry_diseases2). Accessed April 2022.Pathology of Poultry Diseases, lesions of avian diseases.(
Southern African Seabird Colony Diseases Risk assessment: 1–53. Southern African Foundation for the Conservation of Coastal Birds, Cape Town.
International (East Atlantic) Species Action Plan for the Conservation of the Roseate Tern Sterna dougallii (2021–2030): 1–60. European Commission 2021.
The diagnostic value of necropsy. In: Harrison, G. J. & Lightfoot, T. L. (eds.). Clinical Avian Medicine, 2nd Edition: 661–678. Spix Publishing, Florida
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.
Mass mortality among European Common terns in South Africa in April– May 1961. British Birds 55: 103–114.
Structure and function of the avian immune system in birds. Medycyna Weterynaryjna 64: 265–268.
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.
A Review of Mink Predation and Control for Ireland. Irish Wildlife Manuals 40: 1–61.
Difficulties in determining the age of Common Terns in the field. British Birds 94: 268–277.