Abstract
In the context of environmental change, determining the causes underpinning unusual mortality events of vertebrate species is a crucial conservation goal. This is particularly true for polar and sub-polar colonial seabirds, often immunologically naïve to new and emerging diseases. Here, we investigate the patterns of black-browed albatross (Thalassarche melanophris) chick mortality events unrelated to predation recorded between the 2004/05 and 2019/2020 breeding seasons in four colonies across the species range in the Falklands. The prevalence of these mortality events was highly variable across years, causing the death of between 3 and 40% of all chicks in the studied plots. With few exceptions, mortality was patchily distributed. Using clustering methodologies, we identified the spatio-temporal mortality clusters based on the nest locations and chick death date. Using generalised linear models and generalised additive mixed-effects models we found that chicks nearer the first mortality event were predicted to die before those in more distant nests. The probability of death increased with age and was highest for chicks close to nests where a chick had died previously. Our findings, along with the symptoms consistently exhibited by most deceased chicks in the study, strongly suggest the prevalence of a widespread infectious disease, potentially with a common aetiology, both in areas with regular and with very rare human presence. Understanding the causes driving these disease-related mortality events, which seem different from the outbreaks documented in the literature, is a conservation priority for the Falklands black-browed albatross population, which comprises over 70% of the species global population.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The dataset presented here is available for download as electronic supplementary material at https://figshare.com/authors/Francesco_Ventura/7066628
Code availability
The supporting R scripts to reproduce the analysis are available for download as electronic supplementary material at https://figshare.com/authors/Francesco_Ventura/7066628
References
Akaike H (1998) A new look at the statistical model identification. In: Parzen E, Tanabe K, Kitagawa G (eds) Selected papers of hirotugu akaike. Springer, New York, NY, pp 215–222
Birdlife International (2018a) State of the World’s birds: taking the pulse of the planet. BirdLife International, Cambridge, UK
Birdlife International (2018b) Thalassarche melanophris. IUCN Red List Threat Species 2018https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22698375A132643647.en
Boulinier T, Danchin E (1996) Population trends in Kittiwake Rissa tridactyla colonies in relation to tick infestation. Ibis (Lond 1859) 138:326–334. https://doi.org/10.1111/j.1474-919X.1996.tb04345.x
Bourret V, Gamble A, Tornos J et al (2018) Vaccination protects endangered albatross chicks against avian cholera. Conserv Lett 11:1–7. https://doi.org/10.1111/conl.12443
Cairns DK (1988) Seabirds as Indicators of Marine Food Supplies. Biol Oceanogr 5:261–271. https://doi.org/10.1080/01965581.1987.10749517
Cairns DK (1992) Population regulation of seabird colonies. In: Power DM (ed) Current ornithology. Springer, Boston, MA, pp 37–61
Carpenter TE (2001) Methods to investigate spatial and temporal clustering in veterinary epidemiology. Prev Vet Med 48:303–320. https://doi.org/10.1007/s00421-008-0955-8
Catry P, Phillips RA, Forster IP et al (2010) Brood-guarding duration in black-browed albatrosses Thalassarche melanophris: temporal, geographical and individual variation. J Avian Biol 41:460–469. https://doi.org/10.1111/j.1600-048X.2010.05029.x
Catry P, Forcada J, Almeida A (2011) Demographic parameters of black-browed albatrosses Thalassarche melanophris from the Falkland Islands. Polar Biol 34:1221–1229. https://doi.org/10.1007/s00300-011-0984-3
Cori A, Nouvellet P, Garske T et al (2018) A graph-based evidence synthesis approach to detecting outbreak clusters: an application to dog rabies. PLoS Comput Biol 14:1–22. https://doi.org/10.1371/journal.pcbi.1006554
Coulson JC (1968) Differences in the quality of birds nesting in the centre and on the edges of a colony. Nature 217:478–479. https://doi.org/10.1038/217478a0
Cury PM, Boyd IL, Bonhommeau S et al (2011) Global seabird response to forage fish depletion—one-third for the birds. Science 334:1703–1706. https://doi.org/10.1126/science.1212928
Dias MP, Martin R, Pearmain EJ et al (2019) Threats to seabirds: a global assessment. Biol Conserv 237:525–537. https://doi.org/10.1016/j.biocon.2019.06.033
Duffy DC (1983) The ecology of tick parasitism on densely nesting Peruvian seabirds. Ecology 64:110–119. https://doi.org/10.2307/1937334
Ferrer M, Morandini V (2019) Tick infestations correlates at a Falkland Islands Black-browed Albatross colony. Polar Biol 42:625–631. https://doi.org/10.1007/s00300-018-02445-5
Gabriel E, Diggle PJ (2009) Second-order analysis of inhomogeneous spatio-temporal point process data. Stat Neerl 63:43–51. https://doi.org/10.1111/j.1467-9574.2008.00407.x
Gamble A, Garnier R, Jaeger A et al (2019) Exposure of breeding albatrosses to the agent of avian cholera: dynamics of antibody levels and ecological implications. Oecologia 189:939–949. https://doi.org/10.1007/s00442-019-04369-1
Gamble A, Bazire R, Delord K et al (2020) Predator and scavenger movements among and within endangered seabird colonies: Opportunities for pathogen spread. J Appl Ecol 57:367–378. https://doi.org/10.1111/1365-2664.13531
Jaeger J, Lebarbenchon C, Thiebot JB, et al (2015) Diseases of endangered seabirds on Amsterdam island: tracking etiologic agents and introduction of biosecurity measures. In: Second world seabird conference, Cape Town, South Africa, pp 251–252. https://worldseabirdconference.com/wp-content/uploads/2014/02/WSC2-Abstract-Book_rev.pdf
Leotta GA, Chinen I, Vigo GB et al (2006) Outbreaks of avian cholera in Hope Bay, Antarctica. J Wildl Dis 42:259–270. https://doi.org/10.7589/0090-3558-42.2.259
Lyons DE, Roby DD (2011) Validating growth and development of a seabird as an indicator of food availability: captive-reared Caspian Tern chicks fed ad libitum and restricted diets. J F Ornithol 82:88–100. https://doi.org/10.1111/j.1557-9263.2010.00311.x
Major L, La LM, Slade RW et al (2009) Ticks associated with macquarie island penguins carry arboviruses from four genera. PLoS ONE 4:e4375–e4375. https://doi.org/10.1371/journal.pone.0004375
Monaghan P (1996) Relevance of the behaviour of seabirds to the conservation of marine environments. Oikos 77:227–237. https://doi.org/10.2307/3546061
Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23. https://doi.org/10.2307/2332142
Munro G (2007) Outbreak of avian pox virus in gentoo penguins in the Falklands, February 2006. Falklands Conservation, Falkland Islands
Nuttall PA (1984) Tick-borne viruses in seabird colonies. Seabird 7:31–41
Olsén B, Jaenson TG, Noppa L et al (1993) A Lyme borreliosis cycle in seabirds and Ixodes uriae ticks. Nature 362:340–342. https://doi.org/10.1038/362340a0
Olsén B, Duffy DC, Jaenson TG et al (1995) Transhemispheric exchange of Lyme disease spirochetes by seabirds. J Clin Microbiol 33:3270–3274. https://doi.org/10.1128/JCM.33.12.3270-3274.1995
Palmgren H, McCafferty D, Aspán A et al (2000) Salmonella in Sub-Antarctica: low heterogeneity in salmonella serotypes in South Georgian Seals and Birds. Epidemiol Infect 125:257–262. https://doi.org/10.1017/s0950268899004586
Phillips RA, Gales R, Baker GB et al (2016) The conservation status and priorities for albatrosses and large petrels. Biol Conserv 201:169–183. https://doi.org/10.1016/j.biocon.2016.06.017
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6:461–464. https://doi.org/10.1214/aos/1176344136
Scrucca L, Fop M, Murphy TB, Raftery AE (2016) Mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. R J 8:289–317. https://doi.org/10.32614/rj-2016-021
Tickell WLN (2000) Albatrosses. Yale University Press, London
Tickell WLN, Pinder R (1975) Breeding biology of black-browed albatross Diomedea melanophris and grey-headed albatross Diomedea chrysostoma at Bird Island, South Georgia. Ibis (Lond 1859) 117:433–451. https://doi.org/10.1111/j.1474-919X.1975.tb04237.x
Uhart MM, Gallo L, Quintana F (2018) Review of diseases (pathogen isolation, direct recovery and antibodies) in albatrosses and large petrels worldwide. Bird Conserv Int 28:169–196. https://doi.org/10.1017/S0959270916000629
Wang J, Selleck P, Yu M et al (2014) Novel phlebovirus with zoonotic potential isolated from ticks, Australia. Emerg Infect Dis 20:1040–1043. https://doi.org/10.3201/eid2006.140003
Weimerskirch H (2004) Diseases threaten Southern Ocean albatrosses. Polar Biol 27:374–379. https://doi.org/10.1007/s00300-004-0600-x
Weimerskirch H (2016) ACAP Priority Population Assessment—Indian yellow nosed albatross at Amsterdam Island (Indian Ocean). In: Third meeting of the Population and Conservation Status Working Group, La Serena, Chile, 5–6 May 2016
Wolfaardt A (2013) An assessment of the population trends and conservation status of Black-browed Albatrosses in the Falkland Islands. In: First meeting of the population and conservation status workinggroup of the agreement on the conservation of albatrosses and petrels. La Rochelle, France, 29–30 April 2013
Woods R, Jones HI, Watts J et al (2009) Diseases of Antarctic seabirds. In: Kerry KR, Riddle M (eds) Health of Antarctic wildlife: a challenge for science and policy. Springer, Berlin, pp 35–55
Acknowledgements
This work would not have been possible without the help and support of the late Ian Strange, who created the conditions for researchers to work on New Island and who we remember with much gratitude and admiration. Thanks to Maria and Georgina Strange, Dan Birch, Riek van Noordwijk, Nina Dehnhard, Ana Campos, Teresa Catry, Miguel Lecoq, Ana Almeida, Amanda Kuepfer, Caitlin Frankish, Natasha Gillies and Martin Beal for their help. We are grateful to Katie Hampson for her helpful insight into quantitative epidemiological analysis. The New Island Conservation Trust supported field studies on New Island through the supply of research facilities. Thanks to Miguel Ferrer and two anonymous referees for their helpful comments on a previous version of this manuscript.
Funding
This work was funded by the Fundação para a Ciência e a Tecnologia (FCT, Portugal) through the projects: UIDB/04292/2020 and UIDP/04292/2020, granted to MARE; UIDB/50017/2020 and UIDP/50017/2020, granted to CESAM. The Falkland Islands Government provided formal permits and funding through the Environmental Studies Budget.
Author information
Authors and Affiliations
Contributions
PC and JPG designed the research; FV, PC, JPG and RM performed the research and conducted field-work; FV developed the analytical methodology; FV wrote the paper. All authors contributed critically to the drafts and gave final approval for publication.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ventura, F., Granadeiro, J.P., Matias, R. et al. Spatial and temporal aggregation of albatross chick mortality events in the Falklands suggests a role for an unidentified infectious disease. Polar Biol 44, 351–360 (2021). https://doi.org/10.1007/s00300-020-02797-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-020-02797-x