Previous exposure to myxoma virus reduces survival of European rabbits during outbreaks of rabbit haemorrhagic disease

Exploiting synergies among diseases or parasites could increase the efficacy of biological control of invasive species. In Australia, two viruses were introduced to control European rabbits Oryctolagus cuniculus: myxoma virus in 1950 and rabbit haemorrhagic disease virus in 1995. While these biological controls caused initial declines of >95% in affected populations, and despite recurring outbreaks of both diseases, rabbits remain a problem in many areas. We used 18 years of capture–mark–recapture, dead recovery, and antibody assay data from a sentinel population in South Australia to test whether these two diseases interact to modify the survival of individual wild rabbits. We compared four joint, multistate, dead-recovery models to test the hypotheses that rabbit haemorrhagic disease and myxoma viruses have synergistic (i.e., previous exposure to one virus affects survival during outbreaks of the other virus) or additive effects (i.e., previous exposure to one virus does not affect survival during outbreaks of the other virus). Rabbit haemorrhagic disease outbreaks reduced the survival of individuals with no immunity by more than half during the 58-day capture-trip intervals, i.e., from 0.86–0.90 to 0.37–0.48. Myxomatosis outbreaks had a smaller effect, reducing survival to 0.74–0.82; however, myxomatosis outbreaks were more prolonged, spanning more than twice as many trips. There was considerable information-theoretic support (wAIC_c = 0.69) for the model in which exposure to myxomatosis affected survival during rabbit haemorrhagic disease outbreaks. Rabbits previously exposed to myxoma virus had lower survival during rabbit haemorrhagic disease outbreaks than rabbits never exposed to either virus. There was negligible support for the model in which previous exposure to rabbit haemorrhagic disease affected survival in myxomatosis outbreaks (wAIC_c < 0.01). Synthesis and applications. Our results indicate that biological control agents can have a greater impact than single-pathogen challenge studies might suggest. Introducing additional biological control agents might therefore increase the mortality of rabbits beyond the additive effects of individual biological controls. Furthermore, our results show that by understanding and exploiting disease synergies, managers could increase the efficacy of biological controls for other invasive animals.