Exposure of breeding albatrosses to the agent of avian cholera: dynamics of antibody levels and ecological implications
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.
KeywordsCapture–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).
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.
- Anderson RM, May RM (1991) Infectious diseases of humans: dynamics and control. Oxford University Press, OxfordGoogle Scholar
- Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 2015:67Google Scholar
- 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
- Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, BerlinGoogle Scholar
- 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 443:692–695CrossRefGoogle Scholar
- 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
- Keeling MJ, Rohani P (2008) Modeling infectious diseases in humans and animals. Princeton University Press, PrincetonGoogle Scholar
- 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 217:529–537CrossRefGoogle Scholar
- 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