Cross-protection, infection and case fatality rates in wild European rabbits experimentally challenged with different rabbit haemorrhagic disease viruses.

Rabbit haemorrhagic disease virus 2 (RHDV2) is now the dominant calicivirus circulating in wild rabbit populations in Australia. This study compared the infection and case fatality rates of RHDV2 and two RHDVs in wild rabbits, as well as their ability to overcome immunity to the respective other strains. Wild rabbits were allocated to groups either blindly or based on pre-screening for RHDV/RHDV2 antibodies at capture. Rabbits were monitored regularly until their death or humane killing at 7 days post infection. Liver and eyeball samples were collected for lagovirus testing and aging rabbits, respectively. At capture, rabbits showed high seroprevalence to RHDV2 but not to RHDV. In RHDV/RHDV2 seronegative rabbits at capture, infection rates were highest in those inoculated with RHDV2 (81.8%, 18 out of 22), followed by K5 (53.8%, seven out of 13) and CZECH (40.0%, two out of five), but these differences were not statistically significant. In rabbits with previous exposure to RHDV2 at capture, infection rates were highest when inoculated with K5 (59.6%, 31 out of 52) followed by CZECH (46.0%, 23 out of 50), with infection rates higher in younger rabbits for both viruses. In RHDV/RHDV2 seronegative rabbits at capture, case fatality rates were highest for those inoculated with K5 (71.4%), followed by RHDV2 (50.0%) and CZECH (50.0%). In rabbits with previous exposure to RHDV2 at capture, case fatality rates were highest in rabbits inoculated with K5 (12.9%) followed by CZECH (8.7%), with no case fatalities following RHDV2 inoculation. Case fatality rates did not differ significantly between inoculums in either serostatus group at capture. Based on multivariable modelling, time to death post RHDV inoculation increased in rabbits with recent RHDV2 exposure compared with seronegative rabbits and with age. The results suggest that RHDV2 may cause higher mortalities than other variants in seronegative rabbit populations but that K5 may be more effective in reducing rabbit populations in an RHDV2-dominant landscape.

Modeling the distribution of a wide-ranging invasive species using the sampling efforts of expert and citizen scientists.

In its invasive range in Australia, the European rabbit threatens the persistence of native flora and fauna and damages agricultural production. Understanding its distribution and ecological niche is critical for developing management plans to reduce populations and avoid further biodiversity and economic losses.We developed an ensemble of species distribution models (SDMs) to determine the geographic range limits and habitat suitability of the rabbit in Australia. We examined the advantage of incorporating data collected by citizens (separately and jointly with expert data) and explored issues of spatial biases in occurrence data by implementing different approaches to generate pseudo-absences. We evaluated the skill of our model using three approaches: cross-validation, out-of-region validation, and evaluation of the covariate response curves according to expert knowledge of rabbit ecology.Combining citizen and expert occurrence data improved model skill based on cross-validation, spatially reproduced important aspects of rabbit ecology, and reduced the need to extrapolate results beyond the studied areas.Our ensemble model projects that rabbits are distributed across approximately two thirds of Australia. Annual maximum temperatures >25°C and annual minimum temperatures >10°C define, respectively, the southern and northern most range limits of its distribution. In the arid and central regions, close access to permanent water (≤~ 0.4 km) and reduced clay soil composition (~20%-50%) were the major factors influencing the probability of occurrence of rabbits. Synthesis and applications. Our results show that citizen science data can play an important role in managing invasive species by providing missing information on occurrences in regions not surveyed by experts because of logistics or financial constraints. The additional sampling effort provided by citizens can improve the capacity of SDMs to capture important elements of a species ecological niche, improving the capacity of statistical models to accurately predict the geographic range of invasive species.

The Australian National Rabbit Database: 50 yr of population monitoring of an invasive species.

With ongoing introductions into Australia since the 1700s, the European rabbit (Oryctolagus cuniculus) has become one of the most widely distributed and abundant vertebrate pests, adversely impacting Australia's biodiversity and agroeconomy. To understand the population and range dynamics of the species and its impacts better, occurrence and abundance data have been collected by researchers and citizens from sites covering a broad spectrum of climatic and environmental conditions in Australia. The lack of a common and accessible repository for these data has, however, limited their use in determining important spatiotemporal drivers of the structure and dynamics of the geographical range of rabbits in Australia. To meet this need, we created the Australian National Rabbit Database, which combines more than 50 yr of historical and contemporary survey data collected from throughout the range of the species in Australia. The survey data, obtained from a suite of complementary monitoring methods, were combined with high-resolution weather, climate, and environmental information, and an assessment of data quality. The database provides records of rabbit occurrence (689,265 records) and abundance (51,241 records, >120 distinct sites) suitable for identifying the spatiotemporal drivers of the rabbit's distribution and for determining spatial patterns of variation in its key life-history traits, including maximum rates of population growth. Because all data are georeferenced and date stamped, they can be coupled with information from other databases and spatial layers to explore the potential effects of rabbit occurrence and abundance on Australia's native wildlife and agricultural production. The Australian National Rabbit Database is an important tool for understanding and managing the European rabbit in its invasive range and its effects on native biodiversity and agricultural production. It also provides a valuable resource for addressing questions related to the biology, success, and impacts of invasive species more generally. No copyright or proprietary restrictions are associated with the use of this data set other than citation of this Data Paper.

Substantial numerical decline in South Australian rabbit populations following the detection of rabbit haemorrhagic disease virus 2.

Lagovirus europaeus GI.2, also commonly known as rabbit haemorrhagic disease virus 2, was first detected at two long-term monitoring sites for European rabbits, Oryctolagus cuniculus, in South Australia, in mid-2016. Numbers of rabbits in the following 12-18 months were reduced to approximately 20 per cent of average numbers in the preceding 10 years. The impact recorded at the two South Australian sites, if widespread in Australia and persistent for several years, is likely to be of enormous economic and environmental benefit.

Proposal for a unified classification system and nomenclature of lagoviruses.

Lagoviruses belong to the Caliciviridae family. They were first recognized as highly pathogenic viruses of the European rabbit (Oryctolagus cuniculus) and European brown hare (Lepus europaeus) that emerged in the 1970-1980s, namely, rabbit haemorrhagic disease virus (RHDV) and European brown hare syndrome virus (EBHSV), according to the host species from which they had been first detected. However, the diversity of lagoviruses has recently expanded to include new related viruses with varying pathogenicity, geographic distribution and host ranges. Together with the frequent recombination observed amongst circulating viruses, there is a clear need to establish precise guidelines for classifying and naming lagovirus strains. Therefore, here we propose a new nomenclature based on phylogenetic relationships. In this new nomenclature, a single species of lagovirus would be recognized and called Lagovirus europaeus. The species would be divided into two genogroups that correspond to RHDV- and EBHSV-related viruses, respectively. Genogroups could be subdivided into genotypes, which could themselves be subdivided into phylogenetically well-supported variants. Based on available sequences, pairwise distance cutoffs have been defined, but with the accumulation of new sequences these cutoffs may need to be revised. We propose that an international working group could coordinate the nomenclature of lagoviruses and any proposals for revision.

Environmental effects and individual body condition drive seasonal fecundity of rabbits: identifying acute and lagged processes.

The reproduction of many species is determined by seasonally-driven resource supply. But it is difficult to quantify whether the fecundity is sensitive to short- or long-term exposure to environmental conditions such as rainfall that drive resource supply. Using 25 years of data on individual fecundity of European female rabbits, Oryctolagus cuniculus, from semiarid Australia, we investigate the role of individual body condition, rainfall and temperature as drivers of seasonal and long-term and population-level changes in fecundity (breeding probability, ovulation rate, embryo survival). We built distributed lag models in a hierarchical Bayesian framework to account for both immediate and time-lagged effects of climate and other environmental drivers, and possible shifts in reproduction over consecutive seasons. We show that rainfall during summer, when rabbits typically breed only rarely, increased breeding probability immediately and with time lags of up to 10 weeks. However, an earlier onset of the yearly breeding period did not result in more overall reproductive output. Better body condition was associated with an earlier onset of breeding and higher embryo survival. Breeding probability in the main breeding season declined with increased breeding activity in the preceding season and only individuals in good body condition were able to breed late in the season. Higher temperatures reduce breeding success across seasons. We conclude that a better understanding of seasonal dynamics and plasticity (and their interplay) in reproduction will provide crucial insights into how lagomorphs are likely to respond and potentially adapt to the influence of future climate and other environmental change.

Timing and severity of immunizing diseases in rabbits is controlled by seasonal matching of host and pathogen dynamics.

Infectious diseases can exert a strong influence on the dynamics of host populations, but it remains unclear why such disease-mediated control only occurs under particular environmental conditions. We used 16 years of detailed field data on invasive European rabbits (Oryctolagus cuniculus) in Australia, linked to individual-based stochastic models and Bayesian approximations, to test whether (i) mortality associated with rabbit haemorrhagic disease (RHD) is driven primarily by seasonal matches/mismatches between demographic rates and epidemiological dynamics and (ii) delayed infection (arising from insusceptibility and maternal antibodies in juveniles) are important factors in determining disease severity and local population persistence of rabbits. We found that both the timing of reproduction and exposure to viruses drove recurrent seasonal epidemics of RHD. Protection conferred by insusceptibility and maternal antibodies controlled seasonal disease outbreaks by delaying infection; this could have also allowed escape from disease. The persistence of local populations was a stochastic outcome of recovery rates from both RHD and myxomatosis. If susceptibility to RHD is delayed, myxomatosis will have a pronounced effect on population extirpation when the two viruses coexist. This has important implications for wildlife management, because it is likely that such seasonal interplay and disease dynamics has a strong effect on long-term population viability for many species.

Distribution and prevalence of the Australian non-pathogenic rabbit calicivirus is correlated with rainfall and temperature.

BACKGROUND: Australia relies heavily on rabbit haemorrhagic disease virus (RHDV) for the biological control of introduced European wild rabbits Oryctolagus cuniculus, which are significant economic and environmental pests. An endemic non-pathogenic rabbit calicivirus termed RCV-A1 also occurs in wild rabbits in Australian and provides partial protection against lethal RHDV infection, thus interfering with effective rabbit control. Despite its obvious importance for rabbit population management, little is known about the epidemiology of this benign rabbit calicivirus. METHODS: We determined the continent-wide distribution and prevalence of RCV-A1 by analysing 1,805 serum samples from wild rabbit populations at 78 sites across Australia for the presence of antibodies to RCV-A1 using a serological test that specifically detects RCV-A1 antibodies and does not cross-react with co-occurring RHDV antibodies. We also investigated possible correlation between climate variables and prevalence of RCV-A1 by using generalised linear mixed effect models. RESULTS: Antibodies to RCV-A1 were predominantly detected in rabbit populations in cool, high rainfall areas of the south-east and south-west of the continent. There was strong support for modelling RCV-A1 prevalence as a function of average annual rainfall and minimum temperature. The best ranked model explained 26% of the model structural deviance. According to this model, distribution and prevalence of RCV-A1 is positively correlated with periods of above average rainfall and negatively correlated with periods of drought. IMPLICATIONS: Our statistical model of RCV-A1 prevalence will greatly increase our understanding of RCV-A1 epidemiology and its interaction with RHDV in Australia. By defining the environmental conditions associated with the prevalence of RCV-A1, it also contributes towards understanding the distribution of similar viruses in New Zealand and Europe.

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.

Rabbit haemorrhagic disease: applying Occam's razor to competing hypotheses.

Rabbit haemorrhagic disease virus (RHDV) is a highly virulent lagovirus endemic in Europe and Australasian populations of the European rabbit, Oryctolagus cuniculus. It has also caused several unexplained disease outbreaks in domestic European rabbits in North America. Non-pathogenic spread of RHDV leading to persistent infection which later reactivated has recently been proposed as the cause of overt disease and death of a pet rabbit in Canada, the first confirmed case of Rabbit haemorrhagic disease in that country. We suggest that there is little evidence to support non-pathogenic spread of virulent RHDV, some evidence that is contradictory, and evidence to support a simpler alternative hypothesis. RHDV can be spread over long distances between sparse rabbit populations by fomites or flying insects. Although highly pathogenic, RHDV can be limited in its spread within rabbit populations, or its presence masked by closely related but non-pathogenic lagoviruses which can provide protection against acute disease. In the absence of any evidence from clinical studies to support reactivation of persistent RHDV infection, the simpler explanation seems more likely to be correct.