Longitudinal survey of two serotine bat (Eptesicus serotinus) maternity colonies exposed to EBLV-1 (European Bat Lyssavirus type 1): Assessment of survival and serological status variations using capture-recapture models

Abstract

This study describes two longitudinal serological surveys of European Bat Lyssavirus type 1 (EBLV-1) antibodies in serotine bat (Eptesicus serotinus) maternity colonies located in the North-East of France. This species is currently considered as the main EBLV-1 reservoir. Multievent capture-recapture models were used to determine the factors influencing bat rabies transmission as this method accounts for imperfect detection and uncertainty in disease states. Considering the period of study, analyses revealed that survival and recapture probabilities were not affected by the serological status of individuals, confirming the capacity of bats to be exposed to lyssaviruses without dying. Five bats have been found with EBLV-1 RNA in the saliva at the start of the study, suggesting they were caught during virus excretion period. Among these bats, one was interestingly recaptured one year later and harbored a seropositive status. Along the survey, some others bats have been observed to both seroconvert (i.e. move from a negative to a positive serological status) and serorevert (i.e. move from a positive to a negative serological status). Peak of seroprevalence reached 34% and 70% in site A and B respectively. On one of the 2 sites, global decrease of seroprevalence was observed all along the study period nuanced by oscillation intervals of approximately 2–3 years supporting the oscillation infection dynamics hypothesized during a previous EBLV-1 study in a Myotis myotis colony. Seroprevalence were affected by significantly higher seroprevalence in summer than in spring. The maximum time observed between successive positive serological statuses of a bat demonstrated the potential persistence of neutralizing antibodies for at least 4 years. At last, EBLV-1 serological status transitions have been shown driven by age category with higher seroreversion frequencies in adults than in juvenile. Juveniles and female adults seemed indeed acting as distinct drivers of the rabies virus dynamics, hypothesis have been addressed but their exact role in the EBLV-1 transmission still need to be specified.

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

“…For instance, multi-site cross-sectional data could be integrated with single-site longitudinal data (e.g., Picard-Meyer et al 2011, Robardet et al 2017 to overcome the need of a priori knowledge on the host kinetics of the immune response, which is likely conserved within a species sampled across sites. The cross-sectional estimator can nonetheless be accurate for hosts with short lifespan and/or short antibody level persistence or when informed with reliable a priori knowledge on these parameters.…”

“…We then estimated the survival, seroconversion, and seroreversion probabilities using the integrated estimator based on the best model retained in Robardet et al (2017), in which the resighting probability varies over time: /(. In parallel, during each of the eight capture occasions, n CS (20, 40, or 60) unmarked individuals were randomly captured and used to calculate the seroprevalence at each occasion (corresponding to the simulated cross-sectional data).…”

“…This is, for instance, the case when samples can be collected when accidental capture is frequent (e.g., when using non-targeted capture methods such as mist nets, harp, or Sherman traps; e.g., Robardet et al 2017, Mari€ en et al 2018, or as part of harvesting practices (e.g., Rossi et al 2005), or from the offspring of colonial breeders (e.g., Chambert et al 2012b). Overall, the results highlight that the key elements to determine an optimal sampling design are (1) host species life history, (2) the degree of antibody persistence, and (3) the degree of a priori knowledge and uncertainty on demographic and epidemiologic parameters.…”

“…Nevertheless, implementing longitudinal, or integrated, setups can still be valuable in short-lived species to study processes occurring at smaller time scales (e.g., monthly;Mari€ en et al 2018). The interannual time scale we considered here may be particularly suited to the long-term monitoring of seasonally breeding species or to investigate the potential impact of diseases on longlived populations (e.g., Lachish et al 2007, Robardet et al 2017. The interannual time scale we considered here may be particularly suited to the long-term monitoring of seasonally breeding species or to investigate the potential impact of diseases on longlived populations (e.g., Lachish et al 2007, Robardet et al 2017.…”

“…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.…”