AUSTRALIA AND HUANGLONGBING GAC Beattie1, P Holford1, DJ Mabberley1,2, AM Haigh1 and P Broadbent3 1Centre for Plant and Food Science, University of Western Sydney, Locked Bag 1797, Penrith South DC, New South Wales 1797, Australia; 2 Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, United Kingdom; 3 PO Box 46 Mulgoa, NSW 2745, Australia ABSTRACT Preparations are now underway for potential incursions of huanglongbing and its two known vectors, Diaphorina citri Kuwayama and Trioza erytreae del Guercio, into Australia. These preparations, particularly the development of an incursion management plan (IMP), involve extensive reviews of literature related to the origins of Citrus and huanglongbing, and of host records for the disease and its vectors. This paper briefly discusses issues and aspects of the IMP, including pre- and post-incursion management plans. Key words: Incursion Management Plan (IMP), huanglongbing, Australia INTRODUCTION prepared for the Australian citrus industry (Beattie and Barkley 2009). Preparation of The pathogens that cause huanglongbing the plan has involved a thorough review of (HLB) are not known to occur in Australia host records for the disease and its vectors, neither are the two known vectors of the assessment of likely entry pathways, the disease, the Asiatic citrus psyllid Diaphorina biology of the disease and the vectors, and citri Kuwayama [Hemiptera: Sternorrhyncha: methods to limit the impact of the disease Psylloidea: Psyllidae] and the African citrus should one or both vectors be introduced psyllid Trioza erytreae del Guercio [Hemiptera: to Australia. When the current research Sternorrhyncha: Psylloidea: Triozidae]. Early on HLB began in 2000-2001, and during last century, the Asiatic citrus psyllid was initial preparation of the IMP, it was found in northern Australia, but was assumed that the systematics of the family eradicated by chance between 1916-1922, Rutaceae, the subfamily Aurantioideae, and when all introduced species and hybrids of genera within the Aurantioideae, including the genus Citrus in the Northern Territory Citrus and Murraya, were accurate. It was were destroyed during a successful campaign also assumed that Citrus was native to East to eradicate citrus canker (Xanthomonas Asia and that HLB originated in Citrus in citri subsp. citri (ex Hasse 1915) China. This research questioned the above [Pseudomonadales: Pseudomonadaceae] (Bellis assumptions. This paper gives a brief overview et al. 2005). of the origins of the genus Citrus, the origin Australian citrus entomologists and and spread of HLB, the origins of D. citri, pathologists have been involved in some aspects of the systematics of the collaborative research and technology transfer Rutaceae, some aspects of host records of projects in Asia since 1979. The two most HLB and its vectors, and issues related to recent research projects, funded by the the genera Murraya, Merrillia, Bergera and Australian Centre for International Agricultural Clausena. Also discussed are issues related Research (ACIAR) and the Australian to potential incursions of HLB and one or Department of Innovation, have focused on both of its vectors into Australia. These issues HLB research in Indonesia, Vietnam and include: vulnerability of the Australian citrus China. An incursion management plan (IMP) industry and indigenous germplasm; potential for the disease and its vectors has been entry pathways; post-incursion surveys and 1 responses; cost-sharing agreements; and post- small island to the north-east of mainland incursion management of HLB and its vectors. Papua New Guinea (Bayer et al. 2009). ORIGINS OF CITRUS ORIGIN AND SPREAD OF HUANGLONGBING Beattie et al. (2008) recently hypothesised Beattie et al. (2008) recently summarised that the genus Citrus originated in Australia their views, repeated here, on the origins of and that it dispersed westward in equatorial HLB2. The accepted view, as expressed by currents, to Southeast Asia, when such Zhao (1981), da Graça (1991), Bové (2006), currents exited to the north of what is now and in many other publications, is that HLB Papua New Guinea, and on island terranes originated in China. It is based on three that moved 1000 kilometres eastward across assumptions: (1) that the disease was present the same region (Hall 1997, 2001, 2002). in China in the 1800s (Lin 1956); (2) that Some species may also have been dispersed Reinking (1919), Lee (1921), Tu (1932), and by birds and bats. These hypotheses are based some other authors in China before 1940, on current knowledge of plate tectonics and described symptoms of the disease; and (3) the origins of components of Australasia and that HLB evolved with Citrus. However, Asia (e.g., Veevers et al. 1991, Metcalfe 1998, presence of the disease in China in the 1800s Hall 1997, 2001, 2002, Hartley 2001a, b)1, was based on interviews with farmers and the morphology of Citrus and its relatives technicians between 1947 and 1955 (Lin 1956; as circumscribed by Walter Swingle (Swingle see also Lin and Lin 1990). Symptoms of and Reece 1967), recent re-classifications by maladies described by Reinking (1919) and David Mabberley (Mabberley 2004, Zhang Lee (1921) do not describe HLB, and there et al. 2008), and recent molecular studies is no evidence that HLB evolved with Citrus. (e.g., Samuel et al. 2001, Bayer et al. 2004, It is highly likely that the disease was not Muellner et al. 2007, Bayer et al. 2009). widespread in China before the 1940s and that Muellner et al. (2007) estimated the age of it may not have occurred there before 1930 Rutacaeae as 91 my, the Aurantioideae as 71 as: my, C. glauca as 22 my, and C. japonica and • the first substantive record of the C. trifoliata at 18 my. Bayer et al. (2009) disease appears to have been made showed that the genus comprises two major by Chen Qibao in 1938 (Chen 1943, clades, an Australasian clade comprising Lin 1956), four years after Zhou plants considered by Swingle to be species Yuwen collected D. citri on citrus and of Clymenia and Microcitrus in Papua New other hosts at Lingnan University in Guinea, Eremocitrus and Microcitrus in Guangzhou (see Hoffmann 1936); Australia, and Oxanthera in New Caledonia, • parasitoids were not associated with and an Asiatic clade comprising well-known these psyllid populations (Hoffmann commercial Citrus species and hybrids, and 1936); and species considered by Swingle to be species • Aubert (1990a) recorded information of Fortunella and Poncirus. The molecular on Jiaogan (Tankan) tangor production evidence presented by Bayer et al. (2009) in the Chaoyan district of Guangdong also indicates that the citron, C. medica, the from 1946 and 1990 and noted that first described species of Citrus, and long the first dramatic HLB epidemic considered to be native to India, probably occurred from the late 1950s following originated in Australasia, possibly in Papua use of contaminated trees, and that New Guinea, and that its closest relative is subsequent epidemics were related to C. polyandra (syn. Clymenia polyandra), a natural spread of the disease by D. species native to New Ireland, a relatively citri. 1 Animations of events over the past 55 my can be viewed on the internet (SE Asia Research Group 2006: http://www.gl.rhul.ac.uk/ searg/index.html) 2 These views are being reconsidered in light of recent reports of a fourth ‘species’ of 'Candidatus Liberibacter' being discovered in potato (Solanum tuberosum L.), tomato (S. lycopersicum L.) [Solanales: Solanaceae] and other solanaceous plants in New Zealand in association with the recently introduced potato/tomato psyllid Bactericera (=Paratrioza) cockerelli (Sulc) [Psyllidae], presumably from North and/or Central America: see http://www.biosecurity.govt.nz/pests-diseases/plants/potato-tomato-psyllid.htm. 2 With the possible exception of China, complete its life cycle on this species (Moran HLB symptoms were not recorded in 1968). Synonyms of V. lanceolata include Southeast Asia until after the mid 1940s; in Boscia undulata Thunb., Toddalia lanceolata Indonesia in 1948 (Aubert et al. 1985); in Lam, Vepris querimbensis Klotzsch and Vepris Taiwan about 1950 (Su and Huang 1990); undulata (Thunb.) Verdoorn and CA Smith in the Philippines in 1957 (Martinez and (see Mziray 1992). Z. capense is often cited Wallace 1967); in Thailand in the 1960s as Fagara capensis Thunb., and sometimes as (Schwarz et al. 1973a, b; Aubert 1990c); and F. capense. Non-native African hosts on which in Malaysia in the 1970s (Ko 1988, 1991, T. erytreae can complete its development in Lim et al. 1990). Human-assisted spread of Africa include Citrus species and hybrids, the disease through the Indonesian archipelago Murraya paniculata (L.) Jack and Clausena (Tirtawidjaja 1980) to Papua New Guinea anisata (Willd.) Hook. f. ex Benth. (=Cl. (northern Australasia) took more than 50 inaequalis (DC.) Benth.) (Moran 1968, Hollis years. It was first recorded in Papua New 1984, Aubert 1987b). The latter species is Guinea in the northwest at Vanimo in 2002 a host of the 'Ca. L. africanus' (Korsten et. (Weinert et al. 2004). al. 1996) and is often stated as being native Early Indian records of symptoms to Africa (e.g., Moran 1968, Aubert 1987b, resembling those of the disease seem to OEPP/EPPO 2005). It is, however, native to have been overlooked. These records suggest the Western Ghats of India and the northeast that symptoms resembling those of HLB in part of the Indian subcontinent through to Citrus were observed in the mid 1700s in China, and it has many synonyms (Molino the central provinces of India by Roghoji, 1994). There are no reports of D. citri feeding the Bhonsla Raja of Nagpur (Capoor 1963). or developing on it in Asia. The fact that V. Subsequently, relatively early records in north- lanceolata is the preferred native host of T. western and north-eastern India occurred in erytreae in Africa (Moran 1968) suggests that the 1800s and early 1900s (Bonavia 1888- it is the original host of both T.