Greg Mutze

THE INITIAL IMPACT OF RABBIT HEMORRHAGIC DISEASE ON EUROPEAN RABBIT POPULATIONS IN SOUTH AUSTRALIA

The calicivirus agent for rabbit hemorrhagic disease (RHD) escaped from an island quarantine station to the Australian mainland in October 1995. Within 2 wk it was detected at an established field study site where wild European rabbits (Oryctolagus cuniculus) were being monitored in the Flinders Ranges National Park (South Australia, Australia). During November 1995, RHD reduced the rabbit numbers on the site by 95%. Approximately 3% of the population survived challenge by RHD and developed antibodies. Most of the antibody-positive survivors were 3- to 7-wk-old when challenged. Many rabbits died underground, but counts of rabbit carcasses found on the surface indicated that approximately 1 million rabbits had died above ground in the National Park, and that >30 million rabbits may have died in adjacent areas during the November epidemic.

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.

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.

A rapid survey method for estimating population density of European rabbits living in native vegetation

European rabbits are severe environmental pests in Australia but reporting of density-damage relationships has been hindered by a lack of simple methods to estimate the density of rabbit populations in native vegetation. A methodology for quantifying rabbit densities suitable for use in sparse populations of rabbits in conjunction with surveys of the condition of native vegetation is proposed. Dung pellets were counted in 11 629 regularly-spaced quadrats of 0.1 m2 in semiarid, coastal and cool-temperate areas of southern Australia. Mean pellet counts in latrines and the relationship between dung counts outside of latrines and the proportion of quadrats falling on latrines were quantified. This allowed density of dung pellets to be estimated by using a correction factor for latrines instead of attempting to count all pellets within quadrats that included parts of latrines. Rabbit density was calculated from pellet density based on mean pellet size, pellet breakdown rate and estimates of rabbits’ dry matter intake and digestive efficiency. Results were validated against estimates of rabbit density from long-term studies using a combination of spotlight transect counts and burrow entrance counts. The proposed methodology allows estimates of rabbit density in native vegetation to be obtained from just a few hours work and can be used in conjunction with surveys of the condition of native vegetation to quantify rabbit impacts. This methodology is seen as particularly useful in providing a tool to allow rabbit densities to be estimated and then compared with the thresholds, determined separately, at which damage occurs for given ecosystems.

Recovery of South Australian rabbit populations from the impact of rabbit haemorrhagic disease

Abstract Context. Recovery of Australian rabbit populations from the impact of rabbit haemorrhagic disease virus (RHDV) contrasts with more prolonged suppression of wild rabbits in Europe, and has been widely discussed in the scientific community, but not yet documented in formal scientific literature. The underlying causes of recovery remain unclear, but resistance to RHDV infection has been reported in laboratory studies of wild-caught rabbits. Aims. We document numerical changes in two South Australian wild rabbit populations that were initially suppressed by RHDV, and examine serological data to evaluate several alternative hypotheses for the cause of recovery. Methods. Rabbit numbers were assessed from spotlight transect counts and dung mass transects between 1991 and 2011, and age and RHDV antibody sero-prevalence were estimated from rabbits shot in late summer. Key results. Rabbit numbers were heavily suppressed by RHDV between 1995 and 2002, then increased 5- to 10-fold between 2003 and 2010. During the period of increase, annual RHDV infection rates remained stable or increased slightly, average age of rabbits remained stable and annual rainfall was below average. Conclusions. Rabbit populations recovered but neither avoidance of RHDV infection, gradual accumulation of long-lived RHD-immune rabbits, nor high pasture productivity were contributing factors. This leaves increased annual survival from RHDV infection as the most likely cause of recovery. Implications. Previously documented evidence of resistance to RHDV infection may be of little consequence to post-RHD recovery in rabbit numbers, unless the factors that influence the probability of infection also shape the course of infection and affect survival of infected rabbits.

Does a benign calicivirus reduce the effectiveness of rabbit haemorrhagic disease virus (RHDV) in Australia? Experimental evidence from field releases of RHDV on bait

Context. European rabbits are serious environmental and agricultural pests throughout their range in Australia. Rabbit haemorrhagic disease virus (RHDV) greatly reduced rabbit numbers in arid central Australia but had less impact in cooler, higher-rainfall areas. RHDV-like benign caliciviruses (bCVs) have been implicated in limiting the impact of RHDV in the higher-rainfall regions of Australia and also in Europe. Aims. Experimental releases of RHDV on bait were tested as a means of initiating disease outbreaks. Serological evidence of antibodies to bCVs was examined to determine whether they reduce mortality rates and/or spread of the released RHDV, and how that might influence the effectiveness of future RHDV releases for rabbit management. Methods. Four experimental releases were conducted in high-rainfall and coastal regions of southern Australia. Virus activity was implied from recapture rates and serological changes in marked rabbits, and genetic sequencing of virus recovered from dead rabbits. Changes in rabbit abundance were estimated from spotlight transect counts. Key results. Release of RHDV on bait produced disease outbreaks that challenged almost all animals within the general release area and spread up to 4 km beyond the release sites. Recapture rates were high in marked rabbits that possessed antibodies from previous exposure to RHDV and extremely low amongst rabbits that lacked any detectable antibodies. Rabbits carrying antibodies classified as being due to previous infection with bCVs had recapture rates that were dependent on circulating antibody titre and were ~55% of recapture rates in rabbits with clear antibodies to RHDV. Conclusions. This is the first quantified evidence that antibodies produced against bCVs provide significant protection against RHD outbreaks in field populations of rabbits. Implications. bCVs can greatly reduce the impact of RHDV on wild-rabbit populations in Australia and presumably elsewhere. RHDV can be effectively released on bait although further releases are likely to be of minor or inconsistent benefit for controlling rabbit numbers where bCVs are common.

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.

Efficacy of zinc phosphide, strychnine and chlorpyrifos as rodenticides for the control of house mice in South Australian cereal crops

Replicated field trials were conducted to compare the efficacy of zinc phosphide, strychnine and chlorpyrifos for the control of house mice (Mus domesticus) infesting recently sown wheat crops in South Australia. Bait was prepared using whole-wheat grain or grain-based pellets and broadcast into the crops at 1 kg ha–1. Treatment with zinc phosphide reduced mouse numbers by 98%. Two treatments with strychnine baits, applied 11 days apart, also reduced mouse numbers by 98% with no evidence of bait aversion in mice that survived the initial treatment. On the basis of these and other published results, zinc phosphide is considered an effective alternative to strychnine for control of house mice in cereal crops. Chlorpyrifos baits reduced mouse numbers by less than 10%. The trial began too late in the growing season to prevent substantial mouse damage to seed grain and seedlings. The number of seedlings established at treatment time one month after sowing explained 84% of variation in crop yield. Mouse damage is estimated to have reduced yield by more than 0.5 t ha–1 or 15% of potential yield and cost the grower more than

Estimating density-dependent impacts of European rabbits on Australian tree and shrub populations

30 000 in lost production from the 300-ha study area.

Distribution and Prevalence of the Australian Non-Pathogenic Rabbit Calicivirus Is Correlated with Rainfall and Temperature

Introduced European rabbits, Oryctolagus cuniculus, can severely damage Australian native vegetation but the problem is difficult to quantify because simple methods to estimate rabbit impacts are lacking. Management decision-making is often uncertain because of unknown relationships between rabbit density and damage. We tested simple quantitative sampling methods using belt transects to detect differences in critical characteristics of perennial vegetation communities affected by rabbit browsing: damage to individual juvenile shrubs and trees, and loss of recruitment cohorts. Rabbit density and relative abundance of larger herbivores were estimated from dung pellet density. The prevalence of identifiable rabbit browse on juvenile plants increased with increasing rabbit density and was higher for plant species considered by previous authors to be highly palatable than for moderately palatable or unpalatable species. At densities of ≥0.5 rabbits ha–1, highly palatable plant species were severely damaged as juveniles and cohorts in 0.3–1.0 m height classes and 5–20 mm basal diameter classes were missing. Similar damage became apparent in moderately palatable species at 2 rabbits ha–1 but was rarely seen in unpalatable species. Within species, size cohort evenness was inversely related to the proportion of surviving juveniles with identifiable rabbit damage. The effect of rabbits on native vegetation condition can be recorded in a simple manner suitable for identifying density-damage relationships and changes in vegetation condition over time. It is particularly useful in setting target densities below which rabbits must be managed to maintain natural plant recruitment and ecosystem function in conservation reserves and pastoral grazing properties of southern Australia.