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Oecologia

, Volume 189, Issue 4, pp 939–949 | Cite as

Exposure of breeding albatrosses to the agent of avian cholera: dynamics of antibody levels and ecological implications

  • Amandine GambleEmail author
  • Romain Garnier
  • Audrey Jaeger
  • Hubert Gantelet
  • Eric Thibault
  • Pablo Tortosa
  • Vincent Bourret
  • Jean-Baptiste Thiebot
  • Karine Delord
  • Henri Weimerskirch
  • Jérémy Tornos
  • Christophe Barbraud
  • Thierry Boulinier
Population ecology – original research
First Online:

Abstract

Despite critical implications for disease dynamics and surveillance in wild long-lived species, the immune response after exposure to potentially highly pathogenic bacterial disease agents is still poorly known. Among infectious diseases threatening wild populations, avian cholera, caused by the bacterium Pasteurella multocida, is a major concern. It frequently causes massive mortality events in wild populations, notably affecting nestlings of Indian yellow-nosed albatrosses (Thalassarche carteri) in the Indian Ocean. If adults are able to mount a long-term immune response, this could have important consequences regarding the dynamics of the pathogen in the local host community and the potential interest of vaccinating breeding females to transfer immunity to their offspring. By tracking the dynamics of antibodies against P. multocida during 4 years and implementing a vaccination experiment in a population of yellow-nosed albatrosses, we show that a significant proportion of adults were naturally exposed despite high annual survival for both vaccinated and non-vaccinated individuals. Adult-specific antibody levels were thus maintained long enough to inform about recent exposure. However, only low levels of maternal antibodies could be detected in nestlings the year following a vaccination of their mothers. A modification of the vaccine formulation and the possibility to re-vaccinate females 2 years after the first vaccination revealed that vaccines have the potential to elicit a stronger and more persistent response. Such results highlight the value of long-term observational and experimental studies of host exposure to infectious agents in the wild, where ecological and evolutionary processes are likely critical for driving disease dynamics.

Keywords

Capture–mark–recapture Disease ecology Immuno-ecology Maternal antibodies Seabird Serological dynamics Survival 
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Notes

Acknowledgements

We are grateful to Nicolas Giraud, Marine Bely, Romain Bazire, Rémi Bigonneau, Hélène Le Berre, David Hémery, and Marine Quintin for their help in the field, and Cédric Marteau, Camille Lebarbenchon, and Raul Ramos for help at various stages of the work. We also thank Stéphanie Lesceu and Khadija Mouacha (IDvet, France) and Nelly Lesceau and her team (Ceva Biovac, France) for technical help.

Author contribution statement

TB and RG conceived the idea of this work; TB, RG, AG, JT, KD, HW, and CB designed the study; HG and ET conceived the vaccine and the MAT. JT, TB, AG, AJ, KD, VB, and JBT collected the data; AG ran the ELISA and analyzed the serological data; AG and CB ran the capture–recapture analyses; AG led the writing of the manuscript and all authors contributed substantially to the drafts and gave final approval for publication.

Funding

This work was funded by the French Polar Institute (IPEV programs ECOPATH-1151 and ORNITHOECO-109), the Agence Nationale de la Recherche (project EVEMATA 11-BSV7-003), the Réserve Nationale des Terres Australes Françaises, and the Zone Atelier Antarctique. This paper is a contribution to the Plan National d’Action Albatros d’Amsterdam. AG was supported via a Ph.D. fellowship from French Ministry of Research and VB through a CeMEB LabEx post-doctoral fellowship.

Compliance with ethical standards

Conflict of interest

We declare no conflict of interest.

Permits

The experimental design was approved by the Comité de l’Environnement Polaire (TAAF A-2013-71, A-2014-134, A-2015-107, and A-2016-80) and the French Ministry of Research (04939.03).

Data accessibility

Supplementary data associated with this article can be found on the OSU OREME online repository at  https://doi.org/10.15148/c8256ec7-b5e1-4cc4-8429-7bf6cc79263c.

Supplementary material

442_2019_4369_MOESM1_ESM.pdf (1.7 mb)
Supplementary material 1 (PDF 1693 kb)
442_2019_4369_MOESM2_ESM.pdf (885 kb)
Supplementary material 2 (PDF 886 kb)

References

  1. Ahmad TA, Rammah SS, Sheweita SA, Haroun M, El-Sayed LH (2014) Development of immunization trials against Pasteurella multocida. Vaccine 32:909–917CrossRefPubMedGoogle Scholar
  2. Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, OxfordGoogle Scholar
  3. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 2015:67Google Scholar
  4. Benskin CMH, Wilson K, Jones K, Hartley IR (2009) Bacterial pathogens in wild birds: a review of the frequency and effects of infection. Biol Rev 84:349–373CrossRefPubMedGoogle Scholar
  5. Borremans B, Hens N, Beutels P, Leirs H, Reijniers J (2016) Estimating time of infection using prior serological and individual information can greatly improve incidence estimation of human and wildlife infections. PLoS Comput Biol 12:e1004882CrossRefPubMedPubMedCentralGoogle Scholar
  6. Boulinier T, Staszewski V (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23:282–288CrossRefPubMedGoogle Scholar
  7. Boulinier T, Kada S, Ponchon A, Dupraz M, Dietrich M, Gamble A, Bourret V, Duriez O, Bazire R, Tornos J, Tveraa T, Chambert T, Garnier R, McCoy KD (2016) Migration, prospecting, dispersal? What host movement matters for infectious agent circulation? Integr Comput Biol 56:330–342CrossRefGoogle Scholar
  8. Bourret V, Gamble A, Tornos J, Jaeger A, Delord K, Barbraud C, Tortosa P, Kada S, Thiebot J-B, Thibault E, Gantelet H, Weimerskirch H, Garnier R, Boulinier T (2018) Vaccination protects endangered albatross chicks against avian cholera. Conserv Lett 11:e12443CrossRefGoogle Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, BerlinGoogle Scholar
  10. Buzdugan SN, Vergne T, Grosbois V, Delahay RJ, Drewe JA (2017) Inference of the infection status of individuals using longitudinal testing data from cryptic populations: towards a probabilistic approach to diagnosis. Sci Rep 7:1111CrossRefPubMedPubMedCentralGoogle Scholar
  11. Choquet R, Lebreton J-D, Gimenez O, Reboulet A-M, Pradel R (2009a) U-CARE: utilities for performing goodness of fit tests and manipulating capture–recapture data. Ecography 32:1071–1074CrossRefGoogle Scholar
  12. Choquet R, Rouan L, Pradel R (2009b) Program E-SURGE: a software application for fitting multievent models. Modeling demographic processes in marked populations. Springer, Berlin, pp 845–865CrossRefGoogle Scholar
  13. Choquet R, Sanz-Aguilar A, Doligez B, Nogué E, Pradel R, Gustafsson L, Gimenez O (2013) Estimating demographic parameters from capture–recapture data with dependence among individuals within clusters. Methods Ecol Evol 4:474–482CrossRefGoogle Scholar
  14. Christensen JP, Bisgaard M (2000) Fowl cholera. Rev Sci Tech (Int Office Epizoot) 19:626–637CrossRefGoogle Scholar
  15. Cizauskas CA, Bellan SE, Turner WC, Vance RE, Getz WM (2014) Frequent and seasonally variable sublethal anthrax infections are accompanied by short-lived immunity in an endemic system. J Anim Ecol 83:1078–1090CrossRefPubMedPubMedCentralGoogle Scholar
  16. Curtis PE (1983) Transmission of Pasteurella multocida infection from the brown rat (Rattus norvegicus) to domestic poultry. Vet Rec 113:133–134CrossRefPubMedGoogle Scholar
  17. Cuthbert R, Ryan PG, Cooper J, Hilton G (2003) Demography and population trends of the Atlantic yellow-nosed albatross. Condor 105:439–452CrossRefGoogle Scholar
  18. Descamps S, Jenouvrier S, Gilchrist HG, Forbes MR (2012) Avian cholera, a threat to the viability of an Arctic seabird colony? PLoS One 7:e29659CrossRefPubMedPubMedCentralGoogle Scholar
  19. Fridolfsson A-K, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30:116–121CrossRefGoogle Scholar
  20. Garnier R, Graham AL (2014) Insights from parasite-specific serological tools in eco-immunology. Integr Comp Biol 54:363–376CrossRefPubMedGoogle Scholar
  21. Garnier R, Ramos R, Staszewski V, Militão T, Lobato E, González-Solís J, Boulinier T (2012) Maternal antibody persistence: a neglected life-history trait with implications from albatross conservation to comparative immunology. Proc R Soc Lond B Biol Sci 279:2033–2041CrossRefGoogle Scholar
  22. Garnier R, Boulinier T, Gandon S (2013) Evolution of the temporal persistence of immune protection. Biol Lett 9:20130017CrossRefPubMedPubMedCentralGoogle Scholar
  23. Garnier R, Ramos R, Sanz-Aguilar A, Poisbleau M, Weimerskirch H, Burthe S, Tornos J, Boulinier T (2017) Interpreting ELISA analyses from wild animal samples: some recurrent issues and solutions. Funct Ecol 31:2255–2262CrossRefGoogle Scholar
  24. Gasparini J, McCoy KD, Tveraa T, Boulinier T (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol Lett 5:519–524CrossRefGoogle Scholar
  25. Gilbert AT, Fooks AR, Hayman DTS, Horton DL, Müller T, Plowright R, Peel AJ, Bowen R, Wood JLN, Mills J, Cunningham AA, Rupprecht CE (2013) Deciphering serology to understand the ecology of infectious diseases in wildlife. EcoHealth 10:298–313CrossRefPubMedGoogle Scholar
  26. Grindstaff JL (2010) Initial levels of maternally derived antibodies predict persistence time in offspring circulation. J Ornithol 151:423–428CrossRefGoogle Scholar
  27. Haydon DT, Randall DA, Matthews L, Knobel DL, Tallents LA, Gravenor MB, Williams SD, Pollinger JP, Cleaveland S, Woolhouse MEJ, Sillero-Zubiri C, Marino J, Macdonald DW, Laurenson MK (2006) Low-coverage vaccination strategies for the conservation of endangered species. Nature 443:692–695CrossRefPubMedGoogle Scholar
  28. Iverson SA, Gilchrist HG, Soos C, Buttler EI, Harms NJ, Forbes MR (2016) Injecting epidemiology into population viability analysis: avian cholera transmission dynamics at an Arctic seabird colony. J Anim Ecol 85:1481–1490CrossRefPubMedGoogle Scholar
  29. Jaeger A, Lebarbenchon C, Bourret V, Bastien M, Lagadec E, Thiebot J-B, Boulinier T, Delord K, Barbraud C, Marteau C, Dellagi K, Tortosa P, Weimerskirch H (2018) Avian cholera outbreaks threaten seabird species on Amsterdam Island. PLoS One 13:e0197291CrossRefPubMedPubMedCentralGoogle Scholar
  30. Jouventin P, Roux J-P, Stahl J-C, Weimerskirch H (1983) Biologie et frequence de reproduction chez l’albatros à bec jaune (Diomedea chlororhynchos). Le Gerfaut 73(2):161–171Google Scholar
  31. Keeling MJ, Rohani P (2008) Modeling infectious diseases in humans and animals. Princeton University Press, PrincetonCrossRefGoogle Scholar
  32. Lebreton J-D, Burnham KP, Clobert J, Anderson DR (1992) Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecol Monogr 62:67–118CrossRefGoogle Scholar
  33. Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000–1015CrossRefPubMedGoogle Scholar
  34. Leotta GA, Chinen I, Vigo GB, Pecoraro M, Rivas M (2006) Outbreaks of avian cholera in Hope Bay, Antarctica. J Wildl Dis 42:259–270CrossRefPubMedGoogle Scholar
  35. Little MP, Heindenreich WF, Guangquan L (2010) Identifiability and redundancy: theoretical considerations. PLoS One 5:e8915CrossRefPubMedPubMedCentralGoogle Scholar
  36. Metcalf CJE, Farrar J, Cutts FT, Basta NE, Graham AL, Lessler J, Ferguson NM, Burke DS, Grenfell BT (2016) Use of serological surveys to generate key insights into the changing global landscape of infectious disease. Lancet 388:728–730CrossRefPubMedPubMedCentralGoogle Scholar
  37. Mulangu S, Alfonso VH, Hoff NA, Doshi RH, Mulembakani P, Kisalu NK, Okitolonda-Wemakoy E, Kebela BI, Marcus H, Shiloach J, Phue J-N, Wright LL, Muyembe-Tamfum J-J, Sullivan NJ, Rimoin AW (2018) Serologic evidence of ebolavirus infection in a population with no history of outbreaks in the Democratic Republic of the Congo. J Infect Dis 217:529–537CrossRefPubMedPubMedCentralGoogle Scholar
  38. Österblom H, Van Der Jeugd HP, Olsson O (2004) Adult survival and avian cholera in common guillemots Uria aalge in the Baltic Sea. Ibis 146:531–534CrossRefGoogle Scholar
  39. Phillips RA, Gales R, Baker GB, Double MC, Favero M, Quintana F, Tasker ML, Weimerskirch H, Uhart M, Wolfaardt A (2016) The conservation status and priorities for albatrosses and large petrels. Biol Conserv 201:169–183CrossRefGoogle Scholar
  40. Plumb G, Babiuk L, Mazet J, Olsen S, Rupprecht C, Pastoret PP, Slate D (2007) Vaccination in conservation medicine. Rev Sci Tech (Int Office Epizoot) 26:229–241CrossRefGoogle Scholar
  41. Ramos R, Garnier R, González-Solís J, Boulinier T (2014) Long antibody persistence and transgenerational transfer of immunity in a long-lived vertebrate. Am Nat 184:764–776CrossRefPubMedGoogle Scholar
  42. Rivalan P, Barbraud C, Inchausti P, Weimerskirch H (2010) Combined impacts of longline fisheries and climate on the persistence of the Amsterdam Albatross Diomedia amsterdamensis. Ibis 152:6–18CrossRefGoogle Scholar
  43. Rolland V, Barbraud C, Weimerskirch H (2009) Assessing the impact of fisheries, climate and disease on the dynamics of the Indian yellow-nosed albatross. Biol Conserv 142:1084–1095CrossRefGoogle Scholar
  44. Samuel MD, Shadduck DJ, Goldberg DR, Johnson WP (2003) Comparison of methods to detect Pasteurella multocida in carrier waterfowl. J Wildl Dis 39:125–135CrossRefPubMedGoogle Scholar
  45. Samuel MD, Shadduck DJ, Goldberg DR (2005a) Avian cholera exposure and carriers in greater white-fronted geese breeding in Alaska, USA. J Wildl Dis 41:498–502CrossRefPubMedGoogle Scholar
  46. Samuel MD, Shadduck DJ, Goldberg DR, Johnson WP (2005b) Avian cholera in waterfowl: the role of lesser snow and Ross’s geese as disease carriers in the Playa Lakes Region. J Wildl Dis 41:48–57CrossRefPubMedGoogle Scholar
  47. Smith KF, Acevedo-Whitehouse K, Pedersen AB (2009) The role of infectious diseases in biological conservation. Anim Conserv 12:1–12CrossRefGoogle Scholar
  48. Uhart MM, Gallo L, Quintana F (2017) Review of diseases (pathogen isolation, direct recovery and antibodies) in albatrosses and large petrels worldwide. Bird Conserv Int 2017:1–28Google Scholar
  49. Viana M, Mancy R, Biek R, Cleaveland S, Cross PC, Lloyd-Smith JO, Haydon DT (2014) Assembling evidence for identifying reservoirs of infection. Trends Ecol Evol 29:270–279CrossRefPubMedPubMedCentralGoogle Scholar
  50. Weimerskirch H (2004) Diseases threaten Southern Ocean albatrosses. Polar Biol 27:374–379CrossRefGoogle Scholar
  51. Wille M, McBurney S, Robertson GJ, Wilhelm SI, Blehert DS, Soos C, Dunphy R, Whitney H (2016) A pelagic outbreak of avian cholera in North American gulls: scavenging as a primary mechanism for transmission? J Wildl Dis 52:793–802CrossRefPubMedGoogle Scholar
  52. Wobeser GA (1997) Diseases of wild waterfowl. Springer, BostonCrossRefGoogle Scholar
  53. Young HS, Wood CL, Kilpatrick AM, Lafferty KD, Nunn CL, Vincent JR (2017) Conservation, biodiversity and infectious disease: scientific evidence and policy implications. Philos Trans R Soc Lond B Biol Sci 372:20160124CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Amandine Gamble
    • 1
    Email author
  • Romain Garnier
    • 2
  • Audrey Jaeger
    • 3
    • 4
    • 5
  • Hubert Gantelet
    • 6
  • Eric Thibault
    • 6
  • Pablo Tortosa
    • 3
  • Vincent Bourret
    • 1
  • Jean-Baptiste Thiebot
    • 4
    • 7
    • 8
  • Karine Delord
    • 7
  • Henri Weimerskirch
    • 7
  • Jérémy Tornos
    • 1
  • Christophe Barbraud
    • 7
  • Thierry Boulinier
    • 1
  1. 1.Centre d’Écologie Fonctionnelle et Évolutive (CEFE), UMR CNRS 5175University of Montpellier, EPHE, University Paul Valéry Montpellier 3, IRDMontpellierFrance
  2. 2.Department of BiologyGeorgetown UniversityWashingtonUSA
  3. 3.Processus Infectieux en Milieu Insulaire Tropical, UMR CNRS 9192, INSERM 1187, IRD 249, GIP CYROIUniversité de La RéunionSaint DenisFrance
  4. 4.Réserve Naturelle Nationale des Terres Australes FrançaisesSaint PierreFrance
  5. 5.Écologie marine tropicale des océans Pacifique et Indien, UMR IRD 250, CNRSUniversité de la RéunionSaint DenisFrance
  6. 6.Ceva BiovacBeaucouzéFrance
  7. 7.Centre d’Études Biologiques de Chizé, UMR CNRS 7372Université La RochelleVilliers en BoisFrance
  8. 8.National Institute of Polar ResearchTachikawaJapan

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