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

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.

Exploring the infection dynamics of a bacterial pathogen on a remote oceanic island reveals annual epizootics impacting an albatross population

“…However, histological analyses revealed necrotic bacterial lesions in the heart, spleen and/or liver together with Gram-negative bacterial sepsis in nine of 21 necropsied albatross nestlings (Figures 2 and S2-3). This further supports the previous microbiological and experimental investigations regarding Pm pathogenicity [6,8,10]. Nest Pm-PCR status showed no spatial structuration at the monthly temporal scale (Figure S4).…”

“…Amsterdam Island notably hosts several endangered seabird species, including the northern rockhopper penguin ( Eudyptes moseleyi ) and three albatross species: the Indian yellow-nosed ( Thalassarche carteri ), the sooty ( Phoebetria fusca ), and the endemic Amsterdam ( Diomedea amsterdamensis ) albatrosses [5]. Local numbers of yellow-nosed albatrosses have severely declined over the past 30 years, mirroring recurrent die-offs of the nestlings from infectious diseases [6,7], while adults do not appear to suffer from the disease [6,8]. Two microbiological studies have substantiated the link between nestling mortalities and infection by the Gram-negative bacterium Pasteurella multocida ( Pm ) [7,9], a bacterial pathogen known to affect wild and domestic birds worldwide [10–13].…”

Protein Deimination and Extracellular Vesicle Profiles in Antarctic Seabirds

“…Numerous studies have examined levels of a range of heavy metal and other contaminants [39,[45][46][47]. Similarly, a range of seabird species have been screened for specific pathogens [48], including for the agent of avian cholera (Pasteurella multocida) [49][50][51][52], avian pox [53] as well as other bacterial [54], viral [55,56] and parasitic infections [57][58][59][60][61]. However, less research has been carried out on immunological markers, which should be indicative of general health in seabirds [62][63][64][65][66].…”

Next‐generation serology: integrating cross‐sectional and capture–recapture approaches to infer disease dynamics

“…This is particularly true for long-lived vertebrates showing seasonal and colonial breeding (such as seabirds, pinnipeds, and chiropterans) and which are often faithful to their breeding or roosting site (e.g., Chambert et al 2012b, Robardet et al 2017, Gamble et al 2019a. This is particularly true for long-lived vertebrates showing seasonal and colonial breeding (such as seabirds, pinnipeds, and chiropterans) and which are often faithful to their breeding or roosting site (e.g., Chambert et al 2012b, Robardet et al 2017, Gamble et al 2019a.…”

“…In some species, individuals can be marked and repeatedly (re)captured across time, allowing longitudinal sampling. This is particularly true for long‐lived vertebrates showing seasonal and colonial breeding (such as seabirds, pinnipeds, and chiropterans) and which are often faithful to their breeding or roosting site (e.g., Chambert et al , Robardet et al , Gamble et al ). In these systems, capture–recapture approaches have started to be used to estimate epidemiological state transition probabilities (e.g., from healthy to symptomatic) while accounting for recapture probabilities below unity, which are unavoidable in wild settings (Jennelle et al , Conn and Cooch ).…”