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Lethal Biological Control of Rabbits–The Most Powerful Tools For Lethal biological control of rabbits – the most powerful tools for landscape-scale mitigation of rabbit impacts in Australia Tanja Strive1,2* and Tarnya E. Cox2,3 1Commonwealth Scientific and Industrial Research Organisation, Health & Biosecurity, Canberra, ACT, Australia 2Centre for Invasive Species Solutions, Canberra, Australia 3Vertebrate Pests Research Unit, New South Wales Department of Primary Industries, Orange, NSW, Australia Downloaded from http://meridian.allenpress.com/australian-zoologist/article-pdf/40/1/118/2617920/az_2019_016.pdf by guest on 24 September 2021 *Author for correspondence The viral biocontrol agents Myxoma virus (MYXV) and Rabbit Haemorrhagic Disease Virus (RHDV1), released in 1950 and 1996 respectively, are the only control tools to have resulted in significant and lasting landscape-scale suppression of rabbit populations in Australia. Multiple conservation benefits and significant economic savings have resulted from the long-term and widespread reductions in rabbit numbers and impacts. In an effort to ‘boost’ rabbit biocontrol, an additional variant of RHDV1 (’K5’) was recently released nationwide to counteract the decreasing effectiveness of both RHDV1 and MYXV that results from the evolutionary ‘arms race’ between viruses and their hosts. Two years prior to the K5 release, an exotic RHDV strain (RHDV2) appeared in Australia. The commercially available vaccine used to protect pet and farmed rabbits against the officially released K5 was ineffective against the exotic RHDV2, resulting in numerous deaths of domestic rabbits. This created substantial confusion about which strain was released as a biocontrol tool, as well as renewed concerns amongst pet rabbit owners and rabbit farmers about the use of viruses as lethal rabbit control tools in general. Ongoing effective control of wild rabbits in Australia is absolutely essential to protect the substantial conservation gains made by the long-term suppression of rabbit numbers over the past decades, and there is currently no alternative population control tool to achieve this at the required landscape scale. Vaccine formulations need updating to protect non-target farmed and pet rabbits from circulating field variants, including RHDV2, and to increase public acceptance for the ongoing use of viral biocontrol for feral rabbit populations. ABSTRACT Key words: RHDV, pest, biocontrol, virus, rabbit, population, control, feral, impact, community, disease DOI: https://doi.org/10.7882/AZ.2019.016 Introducing wild rabbits to ever recorded colonisations of a vertebrate invasive species Australia: a genuinely bad idea (Stodart and Parer 1988). Their reproductive prowess, combined with fewer predators and diseases than rabbits Amongst the many introduced vertebrates that have had faced in their country of origin, meant numbers soon built a lasting and devastating effect on Australia’s environment up and caused the historical rabbit plagues of the 1930s. and agriculture, the European rabbit (Oryctolagus cuniculus) Direct competition with native animals, overgrazing, and is perhaps the best known example, and Australia’s struggle soil disturbances leading to the loss of valuable topsoil, against rabbits has been the subject of many books (Fenner wreaked havoc with the Australian environment and and Ratcliffe 1965; Coman 2010; Munday 2017). European destroyed many livelihoods (Coman 2010; Munday 2017). rabbits were brought to Australia with the first fleet While the harvesting of rabbit meat and pelts created new (Peacock & Abbott, 2013) but the main introduction that livelihoods for some, the continental scale of the rabbit led to the continent being overrun by rabbits is believed to problem meant that all attempts at manual local control have been the introduction of a small number of wild type including trapping, fencing, poisoning and shooting, were rabbits from England into Geelong in 1859 (Coman 2010). insufficient to stem the tide (Coman 2010; Munday 2017). Introduced for sport by members of the Naturalisation Society, rabbits soon ran wild and spread across the habitable range. Approximately 70% of the continent, with Biological control of rabbits the exception of the wet tropics and extremely arid areas, Tools were needed that would work at a landscape scale, and were colonised by rabbits within 70 years, one of the fastest a self-disseminating lethal disease appeared to be the most Australian 118 Zoologist volume 40 (1) 2019 Theme Edition: Killing for Conservation Lethal biological control of rabbits promising method to achieve this (Fenner and Ratcliffe 1991 and subjected to extensive efficacy and species- 1965). Other forms of biocontrol were also contemplated specificity testing inside secure containment facilities (and some implemented) including the release of cats at the CSIRO Australian Animal Health Laboratory (successfully) and mongoose (unsuccessfully) into the bush (Lenghaus et al. 1994; Cooke and Fenner 2002; Cooke in Australia (Rolls 1969; Peacock and Abbott 2010), and 2014). Later, experimental assessments involved field the release of mustelids in New Zealand, which precipitated trials conducted on Wardang Island close to the South a suite of other problems (Dowding and Murphy 2001; Australian coast. From there, the virus infamously escaped Parkes and Murphy 2003). Various diseases and parasites in late 1995, likely aided by carrion feeding flies that were suggested and evaluated as control agents, but none can mechanically transmit the virus over great distances appeared suitable for the task until the appearance of by ingesting contaminated rabbit flesh (McColl et al. myxomatosis. The disease emerged when its causative 2002). Attempts to contain the outbreak failed, and the agent, the myxoma virus (MYXV), jumped from its natural virus was subsequently officially released in Australia in host Sylvilagus brasiliensis, a cottontail rabbit native to 1996 (Cooke 2014). A year later RHDV1 was illegally Downloaded from http://meridian.allenpress.com/australian-zoologist/article-pdf/40/1/118/2617920/az_2019_016.pdf by guest on 24 September 2021 the Americas, to the European rabbit, causing severe introduced into New Zealand, where its release had not generalised disease and very high fatality rates in this new been approved by the government (O’Hara 2006). The host. Decades of research ultimately led to the release of the initial spread of RHDV1 across the Australian continent virus in 1950 at two sites near Lake Urana in 1950 (Kerr via insect vectors, and likely also aided by people, was swift 2012). MYXV is transmitted between rabbits via biting (Kovaliski 1998), and the impact substantial. Population insects such as mosquitoes and fleas, and following good declines of >90% were reported in some areas (Mutze et rainfall and resulting abundance in mosquito vectors, the al. 2008), although effectiveness in higher rainfall areas virus started to spread. The initial impact of myxomatosis was lower and in some cases negligible (Cooke et al. 2002; on Australian rabbit populations was substantial, with Richardson et al. 2007). This was later attributed to an case-fatality rates and population reductions of >99% endemic, non-virulent virus related to RHDV1, rabbit reported in some areas (Kerr and Best 1998). However, calicivirus Australia-1 (RCV-A1) that can cause partial within a few years, rabbits developed genetic resistance and transient immunity to lethal RHDV1 infections (Alves et al. 2019), and field strains of MYXV with more (Strive et al. 2010; Strive et al. 2013). moderate grades of virulence started to circulate. Work led by Professor Frank Fenner of the Australian National From an animal welfare perspective, RHDV1 was University discovered that MYXV and its host were considered a much more humane solution for rabbit control co-evolving to maximise transmission via biting insects compared to MYXV, as its extremely high virulence results (Fenner et al. 1994). This led to prolonged disease with high in a short course of disease. RHDV1 kills susceptible virus loads in the skin lesions that allowed a longer window rabbits between 36-72 hours after infection with clinical of time for insect vectors to transmit the disease, and also signs such as fever and lethargy observable for an average leading to increased survival rates of rabbits (Kerr et al. of 12 h prior to death. Sometimes no signs of disease are 2012). This ground breaking work later became the text observed and animals are found without any external signs book example for the evolution of virulence in an emerging of disease (reviewed in Abrantes et al., 2012) (Figure 1). In pathogen (Kerr 2012). Not only did this shift towards a less contrast to MYXV, which within a few years co-evolved virulent form of MYXV lead to rabbit numbers gradually with the host towards more moderate virulence grades, increasing again, it also had severe implications for animal RHDV1 has not been evolving towards an attenuated welfare. The prolonged disease led to the now well-known phenotype. It has been proposed that for RHDV1 the severe clinical signs of myxomatosis with abundant skin rabbit carcass, not the diseased animal, is the main source lesions and secondary bacterial infections often leading to of virus transmission via carrion-feeding flies, resulting blindness, and with a disease duration of several weeks in in selection for high levels of virulence associated with some cases (Kerr 2012) (Figure 1). Notably, in domestic a short duration of disease and high case-fatality levels rabbits not
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