RHDV2 outbreak reduces survival and juvenile recruitment, causing European rabbit population collapse

Abstract

Infectious diseases can cause considerable mortality in vertebrate populations, especially when a new pathogen emerges. Quantifying the impact of diseases on wild populations and dissecting the underlying mechanisms requires longitudinal individual monitoring combining demographic and epidemiologic data. Such longitudinal population studies are rare. Rabbit hemorrhagic disease (RHD) is one of the main causes of the decline in European wild rabbit (Oryctolagus cuniculus) populations. A new genotype of RHD virus (RHDV), called RHDV2 or GI.2, emerged in 2010, posing a new threat to previously weakened populations, particularly as this virus can infect individuals already immune to classical RHDV strains. Taking advantage of intensive monitoring from 2009 to 2014 by physical captures and microchip detections of a semi-captive population of rabbits, we finely assessed the demographic impact of an initial RHDV2 outbreak that occurred in the population and identified the most affected demographic parameters. A multi-event modeling analysis revealed decreased survival in both juveniles and adults in 2011 and 2012, suggesting an RHDV2 outbreak for two consecutive years. The short-term survival benefit of vaccination against classical RHDV strains only during these years, and the recovery of carcasses with RHDV2 detection, supported this hypothesis. Variations in population vaccination coverage also explain the difference in adult survival between the two years of the outbreak. And the transient protective effect of vaccination could explain the prolonged duration of the outbreak. A brief episode of myxomatosis in 2011 seems to have had only a limited impact on the population. During outbreak years, in individuals not recently vaccinated, monthly juvenile survival crashed (0.55), and annual adult survival was three times lower than in normal years (0.21 vs. 0.69). The combination of successive juvenile and adult survival estimates for unvaccinated rabbits during the outbreak years resulted in a very low recruitment rate in the breeding population. Finally, RHDV2 outbreaks appear to have caused mortalities comparable to those caused by older classical RHDV strains and may have a strong demographic impact on wild populations of European rabbit. This work highlights the importance of long-term observational and experimental studies to better understand the impact of epidemics on animal populations.