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. erytreae and 1890, Husain and Nath 1927, Pruthi and HLB. Mani 1945, Asana 1958, Capoor 1963, Fraser HLB was transmitted from V. lanceolata et al. 1966, Chadra et al. 1970). With the to orange or mandarin trees by T. erytreae in benefit of current knowledge, it is clear that one of the European colonies on the southeast the severe symptoms described by Husain coast of Africa and then taken to the Indian and Nath (1927) and Pruthi and Mani (1945) subcontinent in infected plants or budwood and attributed to D. citri were symptoms some 300-500 years ago. It was then acquired now known to be caused by 'Candidatus and spread by D. citri. Spread would also Liberibacter asiaticus'. Husain and Nath have occurred through marcotting and grafting, (1927), not Reinking (1919) or Lee (1921), and enhanced by changes in horticultural were therefore the first authors to describe practices that through increased use of symptoms of HLB. Damage caused by D. citri irrigation and fertilisers within monocultures is much more benign and does not lead to would have led to more abundant and frequent death of trees. growth flushes. The latter would have led We think HLB originated in Africa. to far higher populations of D. citri than T. erytreae, the vector of HLB in Africa, is would have occurred in the insect’s original native to sub-Saharan Africa, and is the only environment. It seems the disease and D. species of Trioza that is known to feed and citri may have been introduced to China in develop on Rutaceae (Hollis 1984; Aubert the early 1930s, on plants, possibly a lemon 1987b). T. erytreae has two native rutaceous variety, shipped directly from India or on hosts in Africa on which it can complete its plants of Indian origin from Southeast Asia. development: Vepris lanceolata (Lam.) G. Don Determining if this may have been related to [Toddalioideae: Toddalieae]; and Zanthoxylum plants imported by commercial nurseries or capense (Thunb.) Harv. [Rutoideae: by scientists based at Lingnan University in Zanthoxyleae] (Moran 1968, Hollis 1984, Guangzhou, is still in process. It has not been Aubert 1987b). The psyllid also feeds on the determined yet when HLB was first recorded native monospecific Calodendrum capense (L. in Vietnam or whether it was present there f.) Thunb. [Rutoideae: Diosmeae], but cannot before it was present in China, but it is of

3 interest to note that Wang (1934) mentioned have noticed it. Further evidence that the Citrus magner ex Hort. (sic), a lemon type psyllid may not have been present in China (C. limonia Osbeck var. nov. wagner), being before 1930 is provided by Luh (1936). introduced to Guangdong by George Groff Luh, in a paper on factors, including pests from the garden of a Mr. Wagner, a French and diseases causing fruit loss in 1935 in resident of Saigon. Zhejiang, did not mention the presence of D. citri or symptoms resembling HLB. ORIGINS OF D. CITRI Information about the two primary parasitoids of D. citri also suggests that the Modern psylloids, including the Diaphorinineae psyllid evolved in India. Both parasitoids were and Triozinae, probably evolved with first described from India, the ectoparasitoid the Sapindales in Gondwana (Hollis 1985, Tamarixia radiata (Waterston) [Hymenoptera: 1987, White and Hodgkinson 1985). The Eulophidae] by Waterston (1922) and the Diaphorineae have an ecological preference for endoparasitoid Diaphorencyrtus aligarhensis dry climates (Hollis 1987). D. citri was first (Shafee, Alam and Agarwal) [Hymenoptera: recorded as a serious pest of citrus in India Encyrtidae] by Shafee et al. (1975). Most by Husain and Nath (1927) who, in describing records of T. radiata4 in Southeast Asia appear the damage it caused, were the first to to be related to intentional introductions (Chiu describe what are now known to be symptoms et al. 1988, Chien et al. 1988, Waterhouse of HLB. In China, the Philippines, Malaya 1998) whereas, records of D. aligarhensis5 or Indonesia in the early to mid 1930s, the appear to be linked to unintentional movement psyllid did not assume such a destructive of parasitised D. citri nymphs on live plants status, as reported in India by Husain and to Taiwan (possibly before 1900) and the Nath (1927) (Clausen 1933, Hoffmann 1936). Philippines, and to natural spread overland Hoffmann and Clausen were both aware of with its host. D. aligarhensis is not, as the destruction wrought by the psyllid in India assumed by Chien et al. (1988, 1989, 1991), (Hoffmann 1936). All evidence supports the native to Taiwan or the Philippines, nor were view of Hollis (1987) who suggested that the any parasitoids found in association with D. psyllid evolved in India in association with a citri populations when the psyllid was first species of Murraya3. recorded in Guangzhou (Hoffmann 1936). D. citri was described in Taiwan Tang (1988) mentioned the introduction of (Kuwayama 1908). Crawford (1919) recorded T. radiata to Fujian in China, but considered it as present in the Philippines, Taiwan, Java, it as possibly indigenous given its wide Malay Archipelago, Bengal, southern India distribution in Fujian, as recorded in surveys and southern China, and noted that Frederick within four years of its introduction. He Muir collected specimens from Macao and also considered it possible that the parasitoid Amboina (Moluccas) in 1906. Clausen (1933) occurred in Taiwan before it was released recorded it as present in China, the Philippine there (Tang 1988) and indigenous in Asia, Islands, Taiwan, Malaya, Dutch East Indies, from Saudi Arabia to China (Tang 1990). Burma, India, and Ceylon. Not verified are Other records do not support this. D. the records from Macau and Ambon, and aligarhensis was present in the Philippines Hoffmann (1936) regarded detection of the in 1968 (Catling 1968, Gavarra and Mercado psyllid in Guangdong in 1934 as the first 1988), but T. radiata was not, and was record of D. citri in China. If it was present introduced in 1988 (Catling 1968, Gavarra in China, it was not widespread as Hoffmann and Mercado 1988, Gavarra et al. 1990). (1936), who commenced his studies on pests Both parasitoids were present in Java in of citrus and other plants in Guangdong in Indonesia in 1987 (Nurhadi 1987). Based on 1926 (Jiang et al. 1935), would presumably comments by Nurhadi (1988), it seems they

3We assume this view was based on the genus Murraya as circumscribed by Swingle and Reece (1967) within the subtribe Clauseneae. 4syns Tetrastichus radiatus Waterson (Waterson 1922, Graham 1987, Tang 1990, Tang and Aubert 1990, Waterhouse 1998) and Tetrastichus indicus Khan and Shafee (Hayat and Shahi 2004). 5syns Aphidencyrtus aligarhensis Shafee, Alam and Agarwal, Aphidencyrtus diaphorinae Myartsera and Tryapitzyn and Psyllaephagus diaphorinae Lin and Tao (Noyes and Hayat 1984, Prinsloo 1985, Tang 1990, Tang and Aubert 1990, Waterhouse 1998).

4 may have been introduced to Indonesia on 2 lists the names of common hybrids (sensu psyllid infested plants. In addition to D. citri, Mabberley). hosts of D. aligarhensis apparently include Diaphorina cardiae Crawford), Diaphorina HOST RECORDS auberti Hollis and Psylla sp. (Tang and Aubert 1990): Diaphorina cardiae, is a junior An important component of any IMP for synonym of Diaphorina aegyptiaca Puton HLB and its vectors is knowledge of the (Burckhardt 1984). hosts of the disease and its vectors. We have thoroughly reviewed the literature to determine SYSTEMATICS OF THE RUTACEAE hosts of the 'Ca. Liberibacter' and whether the vectors, both D. citri and T. erytreae The most widely used taxonomic systems feed and multiply on these plants. The format for classifying citrus are those of Walter we have followed is based on Halbert and Tennyson Swingle (Swingle 1943, Swingle Manjunath (2004) but we have included more and Reece 1967) and Tyozaburo Tanaka details and added what we consider to be (Tanaka 1977). They recognised 16 and 162 valid specific and varietal names for the species, respectively. Their views have led to plants while still citing the names used by widespread confusion in the use of names of authors who published the original records. cultivar groups, inappropriate species status Some papers have mentioned plants for which of hybrids, confusion in the names of true claimed taxonomic relationships are invalid species (Scora 1975, Mabberley 1997), and a or poorly understood and for which verifiable profound misunderstanding of generic limits voucher specimens have not been preserved. (Mabberley 1998). Confusion and turmoil has Many such publications are therefore of been exacerbated by the use of a plethora limited value and potentially misleading. It of species names for apomictic hybrid would appear that all commercially grown clones. There has been no consensus on the species and hybrids of Citrus are hosts of 'Ca. names of these entities and many dubious Liberibacter', but the severity of symptoms synonyms and invalid names are widely used varies with the liberibacter form, whether a in books, journals and, most recently, in tree has flushed during a period of psyllid poorly referenced and inconsistent popular activity (De Lange et al. 1985, Koizumi et and technical internet websites that could al. 1994) and the presence and severity of perpetuate errors ad infinitum. Some papers, Citrus Tristeza Virus (CTV) strains (Martinez including molecular studies, deal with plants and Wallace 1967, Martinez 1972, Bhagabati for which claimed taxonomic relationships and Nariani 1980, Prommintara 1990). There are invalid or poorly understood and for is some variability in the literature, particularly which verifiable voucher specimens have not in sensitivity of mandarin (C. reticulata been preserved. Many such publications are Blanco) and pomelo (C. maxima) varieties, therefore of limited value and may mislead but in general sweet orange (C. × aurantium the unwary. Recent work suggests that the L.), mandarin and grapefruit (C. × aurantium genus Citrus comprises about 25 species L.) are highly sensitive, with true lemon (C. (Mabberley 2004). This view is based on × limon), rough lemon (C. × taitensis) and recent reunification of Eremocitrus, Fortunella, trifoliate orange (C. trifoliata) and its hybrids Microcitrus and Poncirus with Citrus tolerant and the lime (C. aurantiifolia) group (Mabberley 1998, Zhang et al. 2008) and on highly tolerant. molecular studies (Guerra et al. 2000, Samuel Table 3 shows an example of the details et al. 2001, Groppo et al. 2008, Bayer et for the genus Murraya. One of the most al. 2009) that support these reunifications contentious issues is whether species or forms and the inclusion of Clymenia polyandra of Murraya (sensu stricto) are hosts of 'Ca. (Tanaka) Swingle from New Ireland in eastern Liberibacter' and of D. citri. These issues Papua New Guinea and species of Oxanthera are addressed elsewhere in the text. It is of from New Caledonia in Citrus. Table 1 lists interest to note here though that although current names of species (sensu Mabberley), Mu. paniculata is generally regarded as the some 50% of which are Australasian. Table preferred host of D. citri, it was not reported

5 Table 1. Specific and common names of 23 species considered to be true species of the genus Citrus (Rutaceae: Aurantioideae: Aurantieae) and their endemic region(s). Widely cultivated species are in bold.

Species Common names Native region C. amblycarpa (Hassk.) sambal, djerook leemo, nasnaran Malaysia and Indonesia Ochse (a possible hybrid) mandarin, ‘Celebes’ papeda C. australis (Mudie) Planchon Australian round lime, dooja Australia C. australasica F. Mueller Australian finger-lime Australia C. cavaleriei H. Léveillé ex Ichang papeda/lime/lemon China Cavalerie (C. ichangensis Swingle) C. fragrans (Montr.) fragrant oxanthera New Caledonia C. garrawayi F. M. Bailey Mount White lime, Garraway’s Australian wild lime Australia C. glauca (Lindley) Burkill Australian desert lime Australia C. gracilis Mabb. Humpty Doo lime Australia C. halimii BC Stone sultan lemon, limau kadangsa, West Malaysia and Sumatera in Indonesia limau kedut kera C. hystrix DC kaffir lime, limau purut, limau hantu Southeast Asia (C. macroptera Montrouz.) C. inodora F. M. Bailey Russell River lime, large-leaf Australia Australian wild lime C. japonica Thunb. syn. Fortunella kumquat China C. medica L. citron Assumed to be India but possibly Papua New Guinea C. maxima (Burm.) Merr. pomelo Indo-China C. neo-caledonica Guill. false orange, large-leaf oxanthera New Caledonia C. oxanthera Beauvisage orange flower oxanthera New Caledonia C. polyandra Tanaka syn. Clymenia New Ireland in Papua New Guinea C. reticulata Blanco mandarin, tangerine, satsuma; China includes C. x suhuiensis Hort. ex Tanaka, known as Canton mandarin, sz-wei-kom, som keo wan, siem, xiem, limau langkat C. trifoliata L. syn. Poncirus trifoliate orange China C. undulata Guill. New Caledonia C. warburgiana F. M. Bailey Milne Bay lime, New Guinea wild lime New Guinea C. wintersii Mabb. syn. Brown River finger lime New Guinea Microcitrus papuana H. F. Winters as a host of the psyllid in India until 1975 to be recorded as a host of the psyllid in (Cheema and Kapur 1975), 60, 41 and 13 India (Fletcher 1917, 1919, Husain and Nath years, respectively, after it was reported 1927). as a host in Taiwan by Maki (1915) and Kuwayama (1931), in China by He and Zhou Murraya, Merrillia and Bergera (1935), and in the Ryukyu Islands of Japan by (Miyatake 1965). Oddly, B. koenigii (cited Murraya sect Murraya, which includes Mu. as Mu. koenigii) was the first Citrus relative paniculata, was recently transferred from the

6 Table 2. Common hybrids within the genus Citrus (Rutaceae: Aurantioideae: Aurantieae). Widely cultivated hybrids are in bold. Hybrid Common name(s) C. x aurantiifolia (Christm.) Swingle lime C. x aurantium L. sour, sweet, Valencia and navel oranges; grape (= C. aurantium L. and C. sinensis (L.) Osbeck) fruit, and king orange/tangor/mandarin, the latter sometimes given as C. nobilis Lour. C. x indica Tanaka Indian wild orange C. x insitorum Mabb. (× Citroncirus webberi J. citrange Ingram and H. E. Moore) C. x limon (L.) Osbeck lemon C. x macrophylla Wester alemow C. x microcarpa Bunge calamondin C. x taitensis Risso (= x jambhiri Lush.) rough lemon C. x latifolia (Yu. Tanaka) Tahitian lime subtribe Clauseneae of the Aurantioideae to Central Java where the susceptibility of Citrus the subtribe Aurantieae (Citreae) and curry spp., Citrus hybrids and some Citrus relatives bush, which But et al. (1984) placed in as host of D. citri and 'Ca. L. asiaticus' Murraya sect Bergera, is once again Bergera was being evaluated. D. citri shows a clear koenigii L., not Mu. koenigii (L.) (Samuel et preference for Mu. exotica rather than for Mu. al. 2001), and remains within the Clauseneae. paniculata at this site (Achmed Hamiwan, Bergera may be junior synonym of Clausena, UGM, pers. comm.), and symptoms of HLB and Samuel et al. (2001) provided molecular have also been observed in Mu. exotica evidence to support the return of the following confirmed inoculation with 'Ca. monospecific Merrillia caloxylon (Ridley) L. asiaticus' (Siti Subandiyah and Achmed Swingle to Murraya sect Murraya. Hamiwan, UGM, pers. comm.). Li and Ke Confusion surrounds the status of Mu. (2002) reported detection of the pathogen in paniculata and Mu. exotica L. There may Mu. paniculata, but it is possible that the be a single highly variable species (Mu. plants used in their study were Mu. exotica. paniculata), the latter and a hybrid (Mu. Likewise, recent extensive records of Mu. exotica), or two species (Mu. paniculata and paniculata as a host of 'Ca. L. asiaticus' and Mu. exotica), as the validity of Mu. exotica 'Ca. L. americanus' in Brazil (Lopes 2006, as a species is uncertain (see Stone 1985, Lopes et al. 2006a,b) may actually pertain Brophy et al. 1994, Mabberley 1998, Ranade to Mu. exotica (Silvio Lopes and Andrew et al. 2006). There may be other, undescribed, Beattie, pers. discussions, December 2006). species. Most Murraya observed by Beattie with Phytochemical differences between Mu. colleagues in Guangzhou, Guangdong, resemble paniculata and Mu. exotica were reported Mu. exotica (sensu Stone 1985), and plants by Li et al. (1988). In our ACIAR project, sent from the Xishuangbana Botanic Gardens significant differences in morphology and in Yunnan to Indonesia for our studies were, molecular biology have been detected between although being labelled Mu. paniculata, them using RAPD analysis (Inggit Puji Astuti, closely resembled Mu. exotica according to Universitas Gadjah Mada (UGM), pers. their morphology and molecular biology. comm.). At this point, what is considered Plants from the University of California, to be Mu. exotica (sensu Stone 1985) is Riverside, again labelled Mu. paniculata were growing and flowering more prolifically than also found by the same methods to be Mu. Mu. paniculata (sensu Stone 1985) at one exotica (Inggit Puji Astuti, Indonesian Botanic of the ACIAR project’s experiment sites in Gardens, Bogor, pers. comm.).

7 Table 3. Host records for huanglongbing and its vectors on Murraya: Las = 'Ca. L. asiaticus' and Lam = 'Ca. L. americanus'. Host D. citri T. erytreae 'Ca. Liberibacter' spp. Murraya One of the food-plants in Taiwan Common host with Las: suspicious symptoms: paniculata (Maki 1915, Kuwayama 1931); noted occasional complete external and internal symptoms like as an alternative host (He and Zhou development (Aubert CVPD after vector transmission 1935); many nymphs and adults 1987a,b) (Tirtawidjaja 1981); transmission by observed on plants over several D. citri from infected citrus (based years (Miyatake 1965); new host on internal phloem degeneration, (Cheema and Kapur 1975); preferred external mottling and chlorosis, host (Singh and Nimbalkar 1977); and stunting) (Tirtawidjaja 1981); all stages frequently observed in can harbour greening organism Bangladesh (Catling et al. 1978); (Aubert et al. 1985). EM negative; favourable host on ‘green hedge no symptoms (Koizumi et al. 1996); plant’ (Tsai et al. 1984); suitable host not a host (Toorawa 1998); not a in Réunion with up to 11 generations host: no graft transmission from in a laboratory and 10 in the field infected citrus (Dai et al. 2005); (Aubert and Quilici 1984); complete detection of the pathogen by PCR development and a preferred field host (Li and Ke 2002); in field trees at in Asia (Aubert 1987a,b); all stages low rate (Lopes 2006a,b). (Osman and Lim 1992); marked Lam: In field trees and by graft increase in populations (Koizumi et al. transmission (Lopes 2006a,b) 1996); host on which most abundant (Tsai et al. 2000); present in all seasons in Florida (Tsai et al. 2002); preferred host in Florida surveys (Halbert and Manjunath 2004) Murraya Las: no symptoms and no detection paniculata by dot hybridisation after attempted var. graft transmission from sweet paniculata orange infected with Las and Citrus Tristeza Virus (Hung et al. 2000) Murraya breeding field populations in the attacked to slight exotica Philippines (Catling 1968); a host extent (van der plant in China (Huang 1953); all Merwe, 1941) stages present on ‘Kunti or China box’ (Khan and Borle 1989) adult feeding in laboratory cages (Aubert 1990b); marked increases in populations (Koizumi et al. 1996); a preferred host in southern China (Beattie pers. observation, Guangzhou 2006) where, probably erroneously, only M. paniculata has been recorded as a host (see Yang et al. 2006); a host in Okinawa (Yasuda et al. 2005, Nakata 2006).

Many host records for D. citri in China Plant Protection Research Institute in Hanoi, that have been ascribed to Mu. paniculata is working to resolve these issues as part of (see Yang et al. 2006) should have been his PhD ‘Circumscription of Murraya and recorded as Mu. exotica. Clearly, there is Merrillia [Sapindales: Rutaceae: Aurantioideae] an urgent need to resolve the status of Mu. and susceptibility of species and forms to exotica and, if it is a hybrid, its parentage, huanglongbing’ at the University of Western as the issue has important implications for Sydney. management of HLB. Of prime concern is that under field conditions, one or both VULNERABILITY OF THE AUSTRALIAN CITRUS ‘forms’ may be an asymptomatic host of INDUSTRY AND INDIGENOUS GERMPLASM 'Ca. L. asiaticus' either permanently after infection or temporarily. Nguyễn Huy Chung, The vulnerability of the Australian citrus an ACIAR John Allwright Fellow from the industry to HLB and its vectors came from:

8 • Australia’s proximity to the Indonesian other plant material across Torres Strait from Archipelago, where both HLB and D. citri Papua New Guinea; and unregulated landings are endemic, and to Papua New Guinea, of boats carrying citrus from other areas to where their eastern-most distribution is the north of Australia. currently limited to the vicinity of Vanimo The risk of airborne entry of D. citri in north-eastern Papua New Guinea (about from Indonesia, Papua New Guinea and, in 750 km from the border with northern the future the Solomon Islands and other Australia); Pacific islands, should the psyllid spread to • the presence of indigenous species of these locations, can be considered high and Citrus in Northern Territory, Queensland, will increase with the inevitable spread of the New South Wales and South Australia; psyllid through Papua New Guinea. This risk • the widespread occurrence of M. could be greatest when the psyllid reaches paniculata as a vigorous ornamental plant the Milne Bay region on the southeast tip of in gardens; the Papua New Guinea mainland and nearby • the occurrence of wild forms of M. islands. paniculata in coastal and sub-coastal Evidence to support this entry risk as regions of Western Australia, the Northern high can be gleaned from the introduction Territory, and Queensland; of the leucaena psyllid, Heteropsylla cubana • current evidence that suggests that all Crawford [Hemiptera: Psyllidae] into Australia. species and varieties of Citrus are likely Bray and Sands (1987) hypothesised that it to be susceptible to HLB; probably entered Australia on air currents • the location of commercial citrus orchards from the Western Pacific to the northeast of in regions throughout mainland Australia Queensland. It was first recorded in Australia that have climates that are favourable for near Bowen in April 1986, shortly after a 'Ca. L. asiaticus', the pathogen that causes particularly severe cyclone in the area and the Asiatic form of HLB, and its principal within three months the psyllid was recorded vector, D. citri; and near Gympie, more than 10 km from a main • the location of commercial citrus orchards road and some 830 km south of Bowen, and in regions in southern Australia that by mid-October in Brisbane (Bray and Sands have climates that would be suitable in 1987). Bray and Sands (1987) considered most years for 'Ca. L. africanus', the it most likely that the insect was dispersed pathogen that causes the African form of throughout Queensland by wind currents. the disease, and its principal vector, T. Others (Sakamaki 2005, Gottwald et al. 2007) erytreae. have speculated that long-distance movement The greatest threat to the Australian of D. citri is governed by seasonal winds and citrus industry and indigenous species of through riding lower jet airstreams (geostrophic Citrus will be from simultaneous incursions movement) associated with summer monsoons of both 'Ca. L. asiaticus' and D. citri and or related to air masses during hurricanes or significant spread by both before detection. tropical storms. Modelling to assess the risk of wind-borne incursions of D. citri could Entry Pathways enable the development of an ‘early warning’ system to alert authorities to a possible The most likely pathways of entry of HLB incursion. and its vectors are illegal introductions of budwood; legal importation of infested or POST-INCURSION SURVEYS infected material that has been inadequately AND RESPONSES treated and/or inspected; passive transport of adult psyllids in commercial and military Draft recommendations for eradication plans, aircraft; air currents (e.g., tropical cyclones and alternative responses, are being prepared and jet-streams) with the potential to carry for the IMP for incursions of HLB and/or its psyllids from the Indonesian Archipelago, vectors. These include: Papua New Guinea and South Pacific islands • recommendations for the establishment to the southeast of Papua New Guinea; of quarantine zones based on scenarios movement of people carrying citrus fruits and related to the climate, topography, size

9 and degree of isolation of locations (e.g., Presence of HLB in the absence of towns, cities and orchards) where citrus its vectors will most probably lead to death and/or alternative hosts of the disease and of infected host plants and the disease its vectors occur, and regions where native would, therefore, not be viewed as a hosts occur naturally; severe threat to the industry. Nonetheless, • guidelines for delimiting surveys, including tree eradication, most probably confined to trace-back and trace-forward analyses; and a small area, should occur as soon as • responses based on where host plants are possible after confirmation of infection. Our located in relation to the initial point of recommendations for eradication of HLB detection. following an incursion and in the presence For situations where eradication of D. of one or both vectors will depend on the citri or T. erytreae in the absence of HLB various scenarios that are being considered, (determined by surveys and PCR-testing of particularly the geographical size of the area fifth instar and adult psyllids) may be feasible, affected, its degree of isolation, and the the following actions can be considered: distributions of infected plants and psyllid • immediate application of recommended infestations within the area. insecticides to all host plants; • skeletonisation of all Citrus trees in Cost Sharing orchards, home gardens and elsewhere (excluding nurseries); In Australia, there is formal cost sharing • skeletonisation of, and removal of all agreement between the Australian citrus leaves from, grafted Citrus trees, and industry and the federal government. destruction of all seedling rootstocks, in The agreement is based on an Emergency nurseries; and Plant Pest (EPP) Response Deed. It allows • elimination of all Murraya, Bergera and the Australian citrus industry to be directly Clausena shrubs and trees. involved in decision making, including Such action should optimise the prospect biosecurity and risk reduction measures. of eradication, as the psyllid cannot survive It also reduces delays in securing funding in the absence of host canopies. Skeletonising, and removes uncertainties and disincentives as an alternative to tree eradication, will for growers to report suspected emergency minimise costs and allow orchards and plant pests. It only deals with responses to nurseries to return to full production sooner. emergency pests covered by a cost sharing It may be feasible to use defoliants in such agreement. The relative share of the total circumstances in orchards to achieve rapid cost of the incursion management that removal of foliage on the psyllid. However, will be covered by the industry and the currently no registered defoliants for citrus government, respectively, varies according to and doses (concentrations and spray volumes) the public and private benefits to be obtained would need to be determined. Outcomes are from eradication. A categorisation group is likely to be variable depending on chemical responsible for determining a cost-sharing rate, spray application method, tree age, water category applicable for high priority pests. relations and environmental conditions at Only emergency pests that have a high impact time of application. It may be possible to or establishment potential are considered for apply defoliants with insecticides, but the categorisation. feasibility of such tank mixes would need to The Government and Plant Industry be carefully considered. Cost Sharing Deed in respect of Emergency Insecticides available for suppressing Plant Pest Responses lists HLB as category psyllid populations include the organo- 2 for which 80% funding for managing an phosphates azinphos-methyl, chlorpyrifos and incursion is provided by the government methidathion, the carbamate carbaryl, and the and 20% by the industry, with the industry neonicotinoid imidacloprid, all of which are component comprising 97.1% from Australian known from overseas reports to be effective Citrus Growers Inc. and 2.9 % from the against the psyllids. Permits for the use of Nursery and Garden Industry Association these chemicals need to be in place before an (PHA National Citrus Industry Biosecurity incursion occurs. Plan: (www.planthealthaustralia.com.au). In the

10 Cost Sharing Categories for Emergency Plant spp. [Solanales: Convolvulaceae]) suggest that Pests, a key criterion for determining the pest natural transmission by these parasitic plants, category is the ‘economic impacts on regions though considered unlikely by Halbert and or the national economy’. The basis for this Manjunath (2004), may be possible. However, criterion is that where there are adverse dodder-covered beds of citrus seedlings were regional impacts from a pest incursion, there observed in a nursery in Pakistan in 2006 is a case for government involvement because by one of the authors of this document, and of the social costs and disruptions that occur budwood for propagation of the seedlings to non-producer stakeholders. Without financial was sourced from an adjacent block of trees commitment from government, producers could in which HLB was prevalent7. Transmission incur the full cost of control measures, whilst via citrus seeds (Tirtawidjaja 1981) at low other non-producer stakeholders could benefit frequencies may also be possible. This could from control measures without contributing to pose risk for propagation of rootstocks by the cost of the control. Additional information seeds from infected trees. Nevertheless, is provided by Barkley and Beattie (2008). such means of transmission would be easily dealt with and would not pose threat to the POST-INCURSION MANAGEMENT OF Australian citrus industry. HUANGLONGBING AND ITS VECTORS Information provided by Ke and Xu (1990) suggests that effective management of Australia is in a fortunate position of being HLB in the presence of D. citri or T. erytreae able to plan and legislate for effective will require annual rates of spread (new management programs before incursions of positive detections) of the disease in orchards HLB and its vectors occur. Biological by either psyllid to be < 0.2% (1 in 500 control will require importation and releases trees), preferably zero. In Australia, particularly of the primary parasitoids of the vectors6, for D. citri, this will only be achieved cost- conditions that favour the survival and activity effectively through area-wide use of pathogen- of these parasitoids and a range of endemic free rootstocks and scions, regular monitoring predators (particularly ladybirds, lacewings and of trees for HLB symptoms, and mandatory spiders), and possible augmentative releases destruction of infected trees immediately after of predators. Greater use of windbreaks will presence of the pathogen is confirmed. Under be required and all nursery trees will need to these circumstances, it may be possible to be propagated in insect-proof screen houses. continue sustainable production of citrus with The timing and synchronisation of flushes and integrated pest management (IPM) programs levels of flushing will need to be carefully based on: managed, where possible, by timing and • biological control; frequency of irrigation, and likewise, fertilisers, • minimal use of strategically timed the latter without jeopardising nutritional applications of mineral oils and systemic requirements of trees. and contact insecticides; and In the absence of D. citri or T. ertyreae, • cultivation, as intercrops or groundcovers, eradication of the HLB should be, as noted of plants that produce volatile repellent above, easily achieved as the pathogens are compounds that slow ingress of D. citri most commonly spread by grafting of infected populations, and therefore HLB, into buds, marcotting (air-layering) (see da Graça orchards. 1991), from tree to tree by root grafting (see At this point, it is envisioned that spray Broadbent et al. 1988). Laboratory experiments programs used in conjunction with mandatory reported by Tirtawidjaja (1981), Garnier and removal of infected trees could comprise one Bové (1983), Olfato et al. (1991), Garnier contact-systemic insecticide in winter before and Bové (1993), Duan et al. (2008) and ‘spring’ growth flush on 20% of trees exceeds observations that the pathogen can multiply lengths of more than 5 mm, and 1-4 contact-systemic and spread within infected dodder (Cuscuta in summer in conjunction with 3-4, 0.25% to 0.5%,

6 The two primary parasitoids of D. citri will need to be introduced from several regions in Asia. 7 These observations suggest that transmission of liberibacter between species, genera and families of plants may occur naturally or at least be possible.

11 horticultural or agricultural mineral oil (preferably • lead to pesticide residues that may exceed nC24 products) sprays commencing when summer- processing, local fresh fruit and export autumn growth flushes ≤ 5 mm are present on 20% MRLs; of trees within blocks of trees of the same age and • reduce orchard biodiversity through impacts cultivar; it may be possible to include fungicides on non-target organisms (invertebrates and in some of these sprays. The aim of such programs vertebrates); would be to kill psyllid eggs, nymphs and adults, and • lead to pesticide resistance in a range of to reduce feeding by adult psyllids and oviposition pests; and by adult females. The insecticides registered for use • increase risks and liabilities for growers on citrus in Australia and suitable for use against and their employees. D. citri are limited and include azinphos-methyl, In the absence of HLB, it should be chlorpyrifos, carbaryl and abamectin. These possible to rely on biological control, possibly insecticides have withholding periods of 14, 14, 3 in conjunction with summer-autumn mineral and 7 days, respectively. Imidacloprid is registered, oil sprays and one to two applications of with a withholding period of 20 weeks, for soil contact-systemic insecticides, for control of applications against citrus leafminer Phyllocnistis D. citri. Less chemical intervention will be citrella Stainton [Lepidoptera: Gracillariidae], required for control of T. erytreae than for D. black citrus aphid Toxoptera citricida (Kirkaldy) citri. [Hemiptera: Aphididae], pink wax scale Ceroplastes In the context of the above, we will rubens Maskell [Hemiptera: Coccidae], and red propose that the Australian citrus industry scale Aonidiella aurantii (Maskell) [Hemiptera: should adopt the following recommendations Diaspididae]. Registered pyrethroids are limited to for control of HLB, and its vectors, in permethrin, bifenthrin and gamma-cyhalothrin. orchards where both the disease and one or It will not be possible to prevent both vectors occur: spread of HLB solely through chemical • use of certified pathogen-free buds suppression of D. citri populations. Limiting produced under a certified budwood rates of spread to acceptable levels through scheme (no use of uncertified buds or such practices will be difficult, probably marcotts); impossible, to achieve and not economically • mandatory area-wide management practices; or environmentally sustainable. Since the • quarterly, or more frequent, monitoring 1970s, the ‘clean and green’ Australian citrus by trained personnel of orchards for industry has been blessed by very effective symptoms of HLB; biological control and IPM programs based • use of PCR or, alternatively, if validated on low pesticide use and relatively stable as appropriate, the iodine-starch test (IST) orchard ecosystems with low pest and in conjunction with microscopy to detect disease pressures (Smith et al. 1997). D. citri phloem degeneration, to confirm HLB management programs based on chemical infection in symptomatic leaves; use will require marked increases in the • mandatory9 and immediate destruction of annual number of pesticide applications8 and HLB-infected trees (those that are PCR or significant improvements in spray application IST positive) by cutting each trunk near (common low-profile airblast sprayers will its base and applying glyphosate to the not achieve required levels of spray coverage stump to kill the roots (this must be done and air turbulence associated with their without waiting to harvest any mature use will enhance dispersal of D. citri and fruit); HLB within orchards). Such programs will, • mandatory and immediate destruction of through destruction of natural enemies, lead to all trees in a block should the percentage increased use of pesticides for control of other of HLB-infected trees in a block reach or pests, particularly scales, mealybugs, thrips exceed 10% of trees within an interval of and mites that currently occur at levels rarely 12 months; requiring chemical intervention. Increased use • mandatory destruction of abandoned of sprays will also: orchards;

8Spray applications per year could easily exceed 10 in cooler regions and 20 or more in warmer regions. 9Legislation will be required for mandatory removal of plants.

12 • mandatory removal of HLB-infected trees • growing plants (as intercrops and/ in home gardens; or ground-covers within orchards) that • mandatory removal of alternative hosts produce volatiles that repel the vectors, of the vectors, particularly species of thereby slowing ingress of HLB into Murraya, Bergera and Clausena, within orchards; close proximity (2 km) of orchards; • timing irrigation (where feasible) and • geographical isolation of budwood sources fertiliser applications to regulate the (mother trees), and their maintenance in timing, number and extent of flush cycles; insect-proof screenhouses; • use of supplementary overhead irrigation • geographical isolation of nurseries from to reduce psyllid populations; and orchards, and of orchards from alternative • education of farm and nursery personnel; hosts of the disease and its vectors; pesticide manufacturers, distributors and • nursery production, in HLB-affected retailers; consultants, technical advisors, regions, in secure insect-proof screen and scouts; research, quarantine, regulatory houses; and advisory staff within government • legislation to prohibit transport of HLB- departments. infected or vector-infested plant parts (e.g., The concept of growing plants that nursery trees, budwood, fruit and seeds) to produce volatiles that repel D. citri, and unaffected areas; thereby slow ingress of HLB, into citrus • management of planting densities, canopy orchards stems from observations and studies dimensions and canopy densities to in southern Vietnam (see Beattie et al. optimise yields per hectare and effective 2006). Evidence to support repellent volatiles application of sprays, and to minimise as the reason for the impacts that have light intensities that favour psyllid been observed in experiments, and in field infestations; observations by Vietnamese farmers, extension • planting of windbreaks to minimise officers and scientists, has been obtained at movement of adult psyllids within and South China Agricultural University (Cen et between orchards; al. in prep., Zaka et al. submitted). Visits by • hedging and pruning practices timed scientists (Tim Gottwald and David Hall, from and undertaken to minimise the risk of the United States Department of Agriculture) enhancing vector populations; and growers (Michael Stewart, Tim Gast and • orchard and nursery management of D. David McCullough) from Florida to Vietnam citri and/or T. erytreae with strategically has led to interest in developing such applied insecticides and mineral oils; technology for use in Florida (see http://www. - timing of sprays should be based fcprac.com/final-priorities-list-design.pdf). on host-plant phenology so as to minimise feeding and oviposition REFERENCES and to maximise mortality of eggs, nymphs and adults; Asana, R.D. 1958. The citrus die-back problem in relation to citrus - application of sprays should be even cultivation in India. Indian Journal of Horticulture 15: 283-286. and thorough, with sprays applied to Aubert, B. 1987a. Epidemiological aspects of the greening run-off; (huanglungbin) disease in Asia. In: The FAO-UNDP Project - use of soil drenches and tree Coordinator in Fuzhou (ed.), Regional Workshop on Citrus injections should be based on tree Greening Huanglungbin Disease, Fuzhou, China, 6–12 size and phenology, and account December 1987. 5 pp. for potential loss or diminution of Aubert, B. 1987b. Trioza erytreae Del Guercio and Diaphorina active ingredient(s) through leaching, citri Kuwayama (Homoptera: Psylloidea) the two vectors of degradation or tree growth; citrus greening disease: biological aspects and possible control • strategies to encourage, where feasible, strategies. Fruits 42: 149-162. biological control of the vectors by Aubert, B. 1990a. High density planting (HDP) of Jiaogan their natural enemies (e.g., planting of mandarine in the lowland area of Shantou (Guangdong groundcover plants to encourage generalist China) and implications for greening control. In: B. Aubert, S. predators); Tontyaporn, D. Buangsuwon (eds), Proceedings of the Fourth

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