, 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


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.


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



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.


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.


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

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)


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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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