Is increased juvenile infection the key to recovery of wild rabbit populations from the impact of rabbit haemorrhagic disease?

The frequency and timing of rabbit haemorrhagic disease (RHD) epizootics and their impact on different age groups of rabbits were studied for 15 years in a recovering rabbit population in South Australia. We recorded the number and body size of rabbits dying during RHD epizootics, collected tissue for genetic analysis of rabbit haemorrhagic disease virus variants and compared the number of carcasses found to the number of susceptible rabbits present at the beginning of each epizootic. All RHD epizootics occurred between late winter and spring, but, progressively, epizootics started earlier and became more frequent and prolonged, fewer susceptible adult rabbits were present during epizootics, and the age of rabbits dying of RHD declined. Increased infection and virus shedding in juvenile rabbits offers the most plausible explanation for those epidemiological changes; the disease is now increasingly transmitted through populations of kittens, starting before young-of-the-year reach adult size and persisting late in the breeding season, so that most rabbits are challenged in their year of birth. These changes have increased juvenile mortality due to RHD but reduced total mortality across all age groups, because age-specific mortality rates are lower in young rabbits than in older rabbits. We hypothesise that this may be the proximate cause of recovery in rabbit populations across Australia and possibly elsewhere.G. J. Mutze, R. G. Sinclair, D. E. Peacock, L. Capucci, J. Kovalisk

RHDV2 overcoming RHDV immunity in wild rabbits (Oryctolagus cuniculus) in Australia

Short CommunicationD. Peacock, J. Kovaliski, R. Sinclair, G. Mutze, A. Iannella, L. Capucc

Rabbit haemorrhagic disease: virus persistence and adaptation in A

Article first published online: 14 AUG 2014In Australia, the rabbit haemorrhagic disease virus (RHDV) has been used since 1996 to reduce numbers of introduced European rabbits (Oryctolagus cuniculus) which have a devastating impact on the native Australian environment. RHDV causes regular, short disease outbreaks, but little is known about how the virus persists and survives between epidemics. We examined the initial spread of RHDV to show that even upon its initial spread, the virus circulated continuously on a regional scale rather than persisting at a local population level and that Australian rabbit populations are highly interconnected by virus-carrying flying vectors. Sequencing data obtained from a single rabbit population showed that the viruses that caused an epidemic each year seldom bore close genetic resemblance to those present in previous years. Together, these data suggest that RHDV survives in the Australian environment through its ability to spread amongst rabbit subpopulations. This is consistent with modelling results that indicated that in a large interconnected rabbit meta-population, RHDV should maintain high virulence, cause short, strong disease outbreaks but show low persistence in any given subpopulation. This new epidemiological framework is important for understanding virus-host co-evolution and future disease management options of pest species to secure Australia's remaining natural biodiversity.Nina I. Schwensow, Brian Cooke, John Kovaliski, Ron Sinclair, David Peacock, Joerns Fickel and Simone Somme

Molecular epidemiology of Rabbit Haemorrhagic Disease Virus in Australia: when one became many

Rabbit Haemorrhagic Disease Virus (RHDV) was introduced into Australia in 1995 as a biological control agent against the wild European rabbit (Oryctolagus cuniculus). We evaluated its evolution over a 16-year period (1995-2011) by examining 50 isolates collected throughout Australia, as well as the original inoculum strains. Phylogenetic analysis of capsid protein VP60 sequences of the Australian isolates, compared with those sampled globally, revealed that they form a monophyletic group with the inoculum strains (CAPM V-351 and RHDV351INOC). Strikingly, despite more than 3000 rereleases of RHDV351INOC since 1995, only a single viral lineage has sustained its transmission in the long-term, indicative of a major competitive advantage. In addition, we find evidence for widespread viral gene flow, in which multiple lineages entered individual geographic locations, resulting in a marked turnover of viral lineages with time, as well as a continual increase in viral genetic diversity. The rate of RHDV evolution recorded in Australia -4.0 (3.3-4.7) × 10(-3) nucleotide substitutions per site per year - was higher than previously observed in RHDV, and evidence for adaptive evolution was obtained at two VP60 residues. Finally, more intensive study of a single rabbit population (Turretfield) in South Australia provided no evidence for viral persistence between outbreaks, with genetic diversity instead generated by continual strain importation.John Kovaliski, Ron Sinclair, Greg Mutze, David Peacock, Tanja Strive, Joana Abrantes, Pedro J . Esteves and Edward C. Holme

Emerging epidemiological patterns in rabbit haemorrhagic disease, its interaction with myxomatosis, and their effects on rabbit populations in South Australia

The impact of rabbit haemorrhagic disease (RHD) on wild rabbit populations was assessed by comparing population parameters measured before the introduction of RHD into Australia in 1995 with population parameters after RHD. We used data from an arid inland area and a moist coastal area in South Australia to examine the timing and extent of RHD outbreaks, their interaction with myxomatosis and their effect on breeding, recruitment and seasonal abundance of rabbits. From this we propose a generalised conceptual model of how RHD affects rabbit populations in southern Australia. RHD decreased long-term average numbers of rabbits by 85% in the arid area. In the coastal area, RHD decreased numbers of rabbits by 73% in the first year but numbers gradually recovered and were only 12% below pre-RHD numbers in the third year. Disease activity generally begins a month or two after the commencement of breeding in autumn or winter, peaks in early spring and ceases to be apparent in summer. Where the disease is most active, the pattern of population change is almost the inverse of the former pattern. During the breeding season, RHD severely suppresses rabbit numbers. Compensatory recruitment of late-born young, protected by maternal antibodies until the disease becomes inactive at the end of spring (also the end of breeding), allows the observed rabbit abundance to increase during summer, albeit to lower levels than before RHD. Maternal antibodies are lost during summer and the population becomes susceptible to RHD. The seasonal peak in myxomatosis activity is pushed back from late spring to early summer or autumn. Survivors of myxomatosis breed after opening rains in autumn but many succumb to RHD before raising their litters. The reduced abundance of rabbits and changed pattern of seasonal abundance have potential consequences for vegetation recovery.Gregory Mutze, Peter Bird, John Kovaliski, David Peacock, Scott Jennings and Brian Cook

Data from: Previous exposure to myxomatosis reduces survival of European rabbits during outbreaks of rabbit haemorrhagic disease

1. Exploiting disease and parasite synergies 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, today rabbits remain a problem in many areas, despite recurring outbreaks of both diseases. 2. We used eighteen 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, multi-state, 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). 3. 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. 4. There was considerable information-theoretic support (wAICc = 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 (wAICc < 0.01). 5. 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 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

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 (wAICc = 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 (wAICc < 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.Louise K. Barnett, Thomas A. A. Prowse, David E. Peacock, Gregory J. Mutze, Ron G. Sinclair, John Kovaliski, Brian D. Cooke, Corey J. A. Bradsha