Introduction and establishment of Exotic Rust Fungi of the order Pucciniales pathogenic on plants of the family Myrtaceae - key threatening process listing
NSW Scientific Committee - final determination
The Scientific Committee, established by the Threatened Species Conservation Act, has made a Final Determination to list the ‘Introduction and establishment of Exotic Rust Fungi of the order Pucciniales pathogenic on plants of the family Myrtaceae’ as a KEY THREATENING PROCESS in Schedule 3 of the Act. Listing of Key Threatening Processes is provided for by Part 2 of the Act.
The Scientific Committee has found that:
1. Exotic disease-causing rusts (basidiomycete fungi of the order Pucciniales, formerly known as the order Uredinales), are known to constitute a major threat to native Australian plants of the Myrtaceae family (Tommerup et al. 2003; Simpson et al. 2006; Plant Health Australia 2009; APPS 2010b; Carnegie et al. 2010). About 50 rusts pathogenic on Myrtaceae have been described on the basis of morphology and epidemiology (Walker 1983; Simpson et al. 2006), but no comprehensive taxonomic studies combining morphological, epidemiological and molecular (DNA) data have yet been made and the true number of distinct taxa remains uncertain. Nearly all are exotic in origin – only two rusts on myrtaceous plants are known to occur naturally in Australia: Puccinia cygnorum R.G. Shivas & J. Walker and Physopella xanthostemonis (J. Walker) J.A. Simpson, K. Thomas & C.A. Grgurinovic. Puccinia cygnorum has been found once on the Western Australian native species Kunzea ericifolia (Simpson et al., 2006), and Physopella xanthostemonis is known from two species of Xanthostemon in the Northern Territory. The remaining rusts of myrtaceous plants are exotic, nearly all from Central and South America.
Within the exotic rusts pathogenic on Myrtaceae, those of greatest immediate risk to Australia’s native biodiversity are members of the rust complex Puccinia psidii Winter sens. lat. (widely known as Eucalyptus Rust or Guava Rust, herein Eucalypt/Guava Rust), native to Central and South America. The taxonomy of this complex is not well understood, and about 20 formal names have been applied here and overseas to variants of the complex (Walker 1983; Simpson et al. 2006). The term ‘variants’, used in this Determination, encompasses entities within the P. psidii sens. lat. complex that are in the literature variously designated as forms, races, biotypes, strains, or morphologically defined species.
One variant of the Puccinia psidii sens. lat
. complex, Uredo rangelii
, distinguished from P. psidii sens. strict
. by morphological differences in the urediniospore stage, has recently arrived and naturalised in Australia, where it is referred to as ‘Myrtle Rust’.
2. The potential threat to the Australian biota of exotic rusts, other than those of the Puccinia psidii sens. lat. complex, is uncertain but all exotic myrtaceous rusts are to be considered part of this Key Threatening Process, and any rusts detected on myrtaceous species in Australia should be regarded as suspect and reported for prompt identification (see www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust).
3. Australia, including its offshore island territories, has 88 genera and about 2253 native species of plants belonging to the family Myrtaceae (CHAH Australian Plant Census, unpublished data, B. Lepschi pers. comm. 24 Aug. 2010), representing around 10% of Australia’s native flora. Myrtaceous plants are ecologically important, and often a frequent to dominant floristic and/or structural element, in very many Australian terrestrial ecological communities, e.g. eucalypt-dominated systems. (The term ‘eucalypts’ denotes the genera Angophora, Corymbia, and Eucalyptus collectively).
Myrtle Rust arrival and naturalisation in Australia
4. In April 2010, a rust subsequently identified as Uredo rangelii J.A. Simpson, K. Thomas & C.A. Grgurinovic (Simpson et al. 2006), a member of the Puccinia psidii sensu lato complex, was found in a planting of Agonis flexuosa cv. 'Afterdark' (Myrtaceae) in a commercial plant production property on the New South Wales Central Coast (Carnegie et al. 2010), although this is unlikely to have been the site of arrival and the extent of infection at another (bushland) site suggests the disease may have been present in Australia for about two years. Uredo rangelii was described (Simpson et al. 2006) from South American specimens bearing uredinia on the non-Australian plant species Myrtus communis (True Myrtle – the type host) and Syzygium jambos (Rose Apple). It was distinguished from the uredinial stage of P. psidii sens. lat. on the basis of differences in the morphology of their urediniospores. A technical description, illustrations of U. rangelii and differences from other rusts of Myrtaceae are available in Simpson et al. (2006). On the basis of the identity of the type host, and to distinguish the disease from that caused by Puccinia psidii sensu stricto, the rust disease caused by U. rangelii is referred to as Myrtle Rust (IPPC 2010; Carnegie et al. 2010). The DNA sequence (rDNA ITS region) of the Australian rust is indistinguishable from that of P. psidii (Carnegie et al. 2010). Since its arrival in Australia, teliospores have been found in its life cycle in the laboratory and in the wild, and it has been found on a taxonomically broad range of new host species. Initially mainly found on cultivated plants in horticultural situations, from late October 2010 the disease began to be detected on wild plants in bushland sites on the NSW Central Coast. By March 2011 Myrtle Rust had been found on more than 40 species of cultivated and wild Australian native plants at many sites along the NSW coast north from Ulladulla, in south-east Queensland, and in the Cairns region of north Queensland. Wet and windy conditions through much of 2010 are thought to have been conducive to reproduction and spread. On 22 December 2010 the National Management Group for Myrtle Rust determined that it was no longer technically feasible to eradicate Uredo rangelii. Fact-sheets on Myrtle Rust are available at www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/uredo-rangelii, and colour photos of symptoms on several affected species are athttp://www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/myrtle-rust-images.
5. Myrtle Rust causes a disease of its host plants which manifests initially as purple or grey to brown lesions (spots) on leaves and sometimes on buds and young stems, developing into pustules with yellow powdery masses of spores (urediniospores), or less conspicuous brownish pustules producing teliospores. Myrtle Rust attacks young growing leaves and shoots, which may become stunted, distorted, or necrotic, and heavy infection may affect the habit and viability of the host plant. The climatic and microclimatic conditions favouring spore germination are likely to be similar to those for Puccinia psidii sens. lat. overseas – see paragraphs 10 and 14 below (NSW Industry & Investment 2010a). The asexual life cycle can be completed in as little as 10 days (NSW Industry & Investment 2010a). Spores of Myrtle Rust can be dispersed (NSW Industry & Investment 2010a) by wind, water-splash, on plant material including seed, on people and their clothing and equipment (NSW Myrtle Rust Weekly Update 3 November 2010, www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/faq, accessed 25 Nov. 2010), and by insects including Honey Bees (Apis mellifera) which work the spore masses (Carnegie et al. 2010). Transport of domestic bee hives is a potential vector for long-distance dispersal into forested areas. Birds and mammals are probable vectors but this has not been confirmed. Spores are thought to be able to remain viable for up to 90 days (NSW Industry & Investment 2010a) on plant material and in the environment.
6. The potential distribution in Australia of Uredo rangelii, and its suitable climatic envelope, are assumed to be as predicted for the general Eucalypt/Guava Rust complex (Puccinia psidii sens. lat. – see paragraph 14 below), and to include most or all of Australia’s eastern seaboard (NSW Industry & Investment 2010a).
7. Wild native plants of New South Wales recorded as infected by U. rangelii as at March 2011 (Industry & Investment NSW, Myrtle Rust update 2 Feb. 2011, http://www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/update, accessed 7 March 2011)) are: Anetholea anisata (Ringwood, Aniseed Myrtle – also known as Syzygium anisatum), Backhousia myrtifolia (Grey Myrtle, Ironwood), Callistemon salignus (Sweet Willow Bottlebrush), Choricarpia leptopetala (Brown Myrtle, Rusty Turpentine), Eucalyptus agglomerata (Blue-leaved Stringybark), Eucalyptus deanei (Mountain Blue Gum), Eucalyptus pilularis (Blackbutt), Lenwebbia prominens (Southern Velvet Myrtle), Leptopspermum rotundifolium (Round-leaved Tea Tree), Melaleuca alternifolia (Tea Tree), Melaleuca quinquenervia (Broad-leaved Paperbark), Rhodamnia maideniana (smooth scrub turpentine), Rhodamnia rubescens (Scrub Turpentine), Rhodamnia whiteana (White Malletwood), Rhodomyrtus psidioides (Native Guava), Syzygium luehmannii (Small-leaved Lilly Pilly, Riberry), Syncarpia glomulifera (Turpentine), and Uromyrtus lamingtonensis.
In Queensland, native host species recorded as at March 2011 include the Endangered Queensland endemic Gossia gonoclada (Angle-stemmed Myrtle), Syzygium apodophyllum (Rex Satinash), and Xanthostemon chrysanthus (Golden Penda).
8. Cultivated Australian native plants recorded as infected by U. rangelii
in New South Wales (Industry & Investment NSW, Myrtle Rust Weekly Update 2 February 2011 http://www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/faq#Myrtle-Rust-weekly-updates, accessed 8 March. 2011) are Acmena
sp. (Lillypilly), Agonis flexuosa
(Willow Myrtle – cultivars ‘Afterdark’, ‘Burgundy’ and ‘Jedda’s Dream’), Backhousia citriodora
(Lemon-scented Myrtle); Callistemon viminalis
(Weeping Bottlebrush), Callistemon
‘St Mary McKillop’, Chamelaucium uncinatum
(Geraldton wax), Gossia inophloia
(Thready Barked Myrtle, formerly Austromyrtus inophloia
– cultivars ‘Aurora’ and ‘Blushing Beauty’), Leptospermum rotundifolium
(Round Leaf Tea-tree), Lophomyrtus bullata
‘Rainbow’s End’, Lophomyrtus x ralphii
cultivars ‘Red Dragon’ ‘Black Stallion’ and ‘Krinkly’, Melaleuca linariifolia
cultivar ‘Claret Tops’, Melaleuca quinquenervia
(Broad-leaved Paperbark), Syncarpia glomulifera
(Turpentine), Syzygium australe
cultivar ‘Meridian Midget’, Syzygium
'Cascade' (S. luehmannii
x S. wilsonii
), and Tristania neriifolia
(Water Gum – initially reported erroneously as “Brush Box”). Exotic species growing in NSW and recorded as infected by U. rangelii
in the same outbreak are the Tahitian exotic Metrosideros collina
varieties identified variously as ‘Dwarf’, ‘Tahiti’ and ‘Fiji’, Myrtus communis
(True Myrtle), Eugenia reinwardtiana
(Beach Cherry), and Syzygium jambos
9. The confirmed host species (in the wild and in cultivation) for the U. rangelii biotype now naturalised in Australia already represent eleven of the 17 currently recognised tribes in the Myrtaceae (following Wilson et al. 2005): tribes Melaleuceae, Backhousieae, Metrosidereae, Tristanieae, Syzygieae, Myrteae, Syncarpieae, Leptospermeae, Xanthostemoneae, Eucalypteae, Chamelaucieae), which suggests a potential for a very wide range of new hosts in Australia. The Australasian Plant Pathology Society (APPS 2010b) states that “there is a real concern that the disease caused by Uredo rangelii (myrtle rust) will not be significantly different to that caused by Puccinia psidii (guava rust)”. Further host testing of native species is underway (S. Kumar, NSW Industry & Investment, in litt. Aug. 2010, pers. comm. Nov. 2010). Infection by inoculation of many additional native species of Myrtaceae under laboratory conditions with the rust variant present in Australia has been demonstrated (DAFF 2010). Native taxa confirmed as susceptible under these conditions (L. Morin, in litt. March 2011) include Acmena smithii, Agonis flexuosa wild type, Allosyncarpia ternata, Angophora costata, A. floribunda, Asteromyrtus magnifica, Austromyrtus dulcis, Backhousia citriodora, Beaufortia schaueri, Beaufortia sparsa, Callistemon ‘Hannah Ray’, Callistemon ‘Kings Park Special’, Callistemon viminalis, Callistemon ‘White Anzac’, Calothamnus quadrifidus, Chamelaucium uncinatum, Corymbia citriodora, C. ficifolia, C. gummifera, C. intermedia, C. maculata, C. tessellaris, C. torelliana, C. variegata, C. variegata x torelliana, Darwinia citriodora, D. glaucophylla, D. procera, Decaspermum humile, Eucalyptus agglomerata, E. camfieldii, E. cladocalyx, E. diversicolor, E. drepanophylla, E. dunnii, E. globulus, E. grandis, E. haemostoma, E. marginata, E. occidentalis, E. olida, E. pellita, E. pilularis, E. populnea, E. resinifera, E. saligna, E. smithii, E. tereticornis, E. tindaliae, E. wandoo, Gossia inophloia, Kunzea ambigua, K. baxteri, K. ericoides, K. pomifera, Leptospermum laevigatum, L. morrisonii, L. polygalifolium, Linsayomyrtus racemoides, Melaleuca alternifolia, M. biconvexa, M. ericifolia, M. linariifolia, M. quinquenervia, Regelia velutina, Syncarpia glomulifera, Syzygium australe ‘Captain Cook’, S. australe ‘Meridian Midget’, S. fibrosum, S. paniculatum, Tristaniopsis laurina, Verticordia chrysantha, Waterhousea floribunda, Xanthostemon chrysanthus.
10. The pre-arrival impact assessments made (Plant Health Australia 2008, 2009) for Puccinia psidii sens. lat. should be regarded as fully applicable to the one variant (Myrtle Rust) that has now naturalised here, i.e. a high potential for entry to Australia, a high establishment potential, a high-to-extreme spread potential, a high environmental impact, and a high-to-extreme economic impact. Field observations suggest variable susceptibility between some of the species affected so far (Carnegie et al. 2010).
Eucalypt/Guava Rust (Puccinia psidii sens. lat.)
11. Puccinia psidii Winter sens. lat. (Eucalypt/Guava Rust), is a pathogen complex identified as a disease of significance in the National Nursery and Garden Industry Biosecurity Plan (Plant Health Australia 2008) and the National Plantation Timber Industry Biosecurity Plan (Plant Health Australia 2007). A national-level Contingency Plan (Plant Health Australia 2009) was used in part for the response to the Myrtle Rust variant in 2010. P. psidii (sens. lat.) has been assessed (Plant Health Australia 2008, 2009) as having a high potential for entry to Australia, a high establishment potential, a high-to-extreme spread potential, a high environmental impact, and a high-to-extreme economic impact.
12. Puccinia psidii sens. lat. is a teleomorphic rust fungus, native to Central and South America, pathogenic on host plants of the family Myrtaceae (sensu Wilson et al. 2005, including the former Heteropyxidaceae), including many eucalypt species. A fact sheet on Eucalypt Rust, with images, is available at www.australasianplantpathologysociety.org.au/Regions/POTM/May10 POTM.pdf. Fuller technical descriptions are available in Plant Health Australia (2009), in works cited by Simpson et al. (2006), and (with images) at www.padil.gov.au/viewPestDiagnosticImages.aspx?id=415. Two methods of molecular diagnosis of P. psidii sens. lat. are available (Langrell et al. 2003; Langrell et al. 2008; Plant Health Australia 2009): a highly sensitive nested PCR test, and a direct (rDNA ITS) sequence comparison test.
13. Numerous taxa within Puccinia psidii sens. lat. (Eucalypt/Guava Rust), including Uredo rangelii (Myrtle Rust), have been described on morphological features (Walker 1983, Simpson 2006) but the complex is poorly studied (Glen et al. 2007) and the true number of taxonomic and epidemiological variants is unknown, although it is clear that Uredo rangelii is distinct in spore morphology and host range from P. psidii sens. strict. The general life cycle is illustrated in Plant Health Australia (2009) and Glen et al. (2007). Simpson et al. (2006) posit an unidentified alternate non-myrtaceous host for the aecial stage of the life cycle, but Glen et al. (2007) regard this as unlikely. Different spore types may be produced, with urediniospores being the most prolific and probably the most dispersible. Urediniospore germination is favoured by high humidity, leaf wetness for more than six hours, darkness, and temperatures of 15-25o C (Glen et al. 2007). The cycle of infection, lesion, and urediniospore production can be as short as 10 days (Plant Health Australia 2009), allowing rapid spread under favourable conditions. Urediniospores can survive for at least some weeks (Aparecido et al. 2003, cited in Plant Health Australia 2009). Glen et al. (2007) cite unpublished work by Lana et al. indicating that urediniospores may remain viable for 90 days under favourable conditions. Teliospores may survive even longer (Glen et al. 2007). Viable spores of P. psidii were detected on a shipment of timber and on the outer surface of an associated container arriving in Australia from Brazil in 2004 (Grgurinovic et al. 2006; Commonwealth of Australia 2006). Urediniospores are reported to be readily dispersed by wind (e.g. Uchida & Loope 2009). Both spore types are dispersed by movement on infected plant material, as contaminants in pollen (Zuaza et al. 2010b; Carnegie et al. 2010), on clothing and personal effects of visitors to infected areas (Langrell et al. 2003, cited in Glen et al. 2007). Movement of the pathogen in batches of plant germplasm (e.g. seed) is possible (Langrell et al. 2008), as is transmission by foraging honeybees and in the transport of bee hives. Transmission of spores by birds and mammals also seems likely.
14. Puccinia psidii in South America causes a usually mild rust disease on a broad range of native host plants belonging to the Myrtaceae. It is however known to be capable of causing severe rust disease in plantations of the non-native guava (Psidium) and of Australian-origin eucalypts, and has been found to establish with greater or lesser disease severity on a wide range of Australian-origin Myrtaceae species under field and/or laboratory conditions, including genera that are ecologically important in Australian ecological communities such as Angophora, Callistemon, Corymbia, Eucalyptus, Kunzea, Melaleuca, Syncarpia and Syzygium (Simpson et al. 2006; Zuaza et al. 2010b). The susceptibility or resistance of myrtaceous plants to infection by P. psidii, and the severity of the resulting disease symptoms, varies with rust biotype, host species, host provenance within-species, and host stage of growth (Plant Health Australia 2009; Zuaza et al. 2010b). Notwithstanding the observed variation, Glen et al. (2007) noted that “pathogens are frequently far more virulent on naive hosts”, and contingency planning (Commonwealth of Australia 2006; Plant Health Australia 2009) has been on the basis that epidemic outbreaks are to be expected if the pathogen establishes in Australia.
15. Disease symptoms on susceptible plants typically include lesions on young, actively growing leaves and shoots, which become conspicuous yellow pustules (uredinia) extruding masses of urediniospores, or less frequent and less conspicuous brownish telia producing heavier teliospores. Lesions may also occur on fruits of fleshy-fruited species. Rust lesions can expose infected tissue to secondary infections from other fungi. Severe rust disease may kill shoot tips, causing loss of leader shoots and altering the plant’s habit to a bushier form, with prolific branching and galling in eucalypt species being a sign of previous rust disease (Plant Health Australia 2009). Very severe infection may cause gross distortion of habit or plant death (Tommerup et al. 2003). Host plants are generally more susceptible at the seedling stage, with older plants and foliage being more resistant; it is not known whether this reflects physiological changes in the older plant, or a less conducive microclimate for rust establishment (Simpson et al. 2006). Zuaza et al. (2010a) note a negative correlation between the height above ground of foliage, and its susceptibility to infection. Coppice growth in some susceptible eucalypt species is reported as very prone to infection (de Carvalho et al. 1994, cited in Simpson et al. 2006; Tommerup et al. 2003), and post-fire epicormic shoots may also be susceptible, although research on this under Australian conditions is lacking (Simpson et al. 2006).
16. Puccinia psidii (Eucalypt/Guava Rust) was recorded as arriving in Florida USA in 1977, infecting new native host species and the introduced Australian species Melaleuca quinquenervia (Glen et al. 2007). In April 2005 it was discovered in Hawaii on the island of Oahu, and in less than a year it had spread to all islands of the Hawaiian group but one, on both introduced species and new Hawaiian native hosts (Uchida et al. 2006; Killgore & Heu 2005; Loope 2010). Dispersal of urediniospores in Hawaii, thought to be by wind, resulted in “heavy infection of even small groups of Syzygium jambos isolated by 1 km or more ... billions of urediniospores covered the ground under infected trees” (Uchida & Loope, 2009).
17. Puccinia psidii sens. lat. (including the Myrtle Rust variant already present in Australia in 2010) is unlikely to establish in arid and semi-arid regions due to its need for high humidity for urediniospore germination (Ruiz et al. 1989, cited in Plant Health Australia 2009). Preliminary bioclimatic modelling for areas of Australia likely to be at high risk of establishment of Puccinia psidii (Booth et al. 2000; Booth & Jovanovic unpublished data in Glen et al. 2007) predict, as a minimum, that most of the eastern seaboard and the eastern fall of the Great Dividing Range, and coastal areas in the Top End of the Northern Territory, are climatically suitable for the rust, subject to the presence of suitable host species and microhabitat. A zone of lower risk extends onto the western slopes of the Divide. The area of highest risk in New South Wales is the coastal zone from the Illawarra north to the Queensland border. This latter area includes a large proportion of the New South Wales conservation reserve system; very many Myrtaceae-dominated communities of heath, woodland and forest; and most of the NSW component of Australia’s World Heritage-listed rainforest, which also has a high proportion of myrtaceous species. Alternative bioclimatic modelling (Plant Health Australia 2009) to define climatic habitat likely to be suitable for the rust for only some years per decade, extends the lower-risk area well west of the Divide in northern New South Wales and southern Queensland, and predicts low to moderate risk areas in some other states. Glen et al. (2007) observed that if P. psidii were to become established in Australia, it “would most likely spread very rapidly over the climatically suitable regions”, and regions outside the mapped risk-areas may also be likely to suffer rust epidemics, perhaps less frequently.
18. Options for physical, chemical and biological control of P. psidii sens. lat. under Australian conditions are canvassed by Glen et al. (2007) and Plant Health Australia (2009), but these options are limited and only likely to be effective for cultivated situations (nurseries, garden areas, and perhaps plantation forests). Management options include eradication at a very early stage of arrival, and measures to minimise the spread of infection (Tommerup et al. 2003; Glen et al. 2007). Selection for resistant genotypes in native species would be slow and unlikely to prevent loss of populations, genotypes, and whole species, resulting in environmental degradation and habitat loss. Susceptible native and exotic species used in urban landscaping, home gardens, plantation forestry and orchards would act as sources of continuing rust propagule pressure on nearby wild plant communities.
19. Only a small proportion of Australian native myrtaceous plant species have yet been tested for their potential to act as hosts for variants of the P. psidii complex, and most have been found to be susceptible to varying degrees (Zuaza 2010b; Plant Health Australia 2009; L. Morin in litt. March 2011). Literature reports summarised in Plant Health Australia (2009) showed that of 83 native Australian species of Myrtaceae from 19 genera tested for susceptibility to P. psidii sens. lat. (variants not documented), 73 species from 16 genera showed some degree of susceptibility in more than 30% of sample plants. The taxa cited in those reports and subsequently as showing infectability - in the wild, in cultivation, or in the laboratory - represent 13 of the 17 tribes currently recognised in the family, suggesting a very broad taxonomic range of potential hosts and an existing broad base of capability for P. psidii variants to infect new host species. If this proportion of susceptibility is found to apply across the Australian Myrtaceous flora, it has been projected that 1447 of Australia’s native species are potential hosts (Plant Health Australia 2009); this estimate is however based on a 1992 estimate of only 1646 native species in the family (2253 are now recognised) and should be considered a significant underestimate of the number of potential hosts. The introduction and establishment in Australia of other variants of P. psidii sens. lat. and of other pathotypes of Uredo rangelii, could greatly increase both the host range and severity of disease effects. The importance of prevention or early eradication of further arrivals of other variants is discussed in the Hawaiian context by Loope (2010).
20. Many of the native plant species known to be susceptible to P. psidii are important constituents of many described ecological communities in forest, woodland, rainforest, and heath vegetation types. Many are also endemic, or nearly so, to regions within the predicted high-risk zones for establishment of P. psidii. Many species and provenances not yet tested may also be susceptible (Zuava et al. 2010b). Susceptibility and resistance have generally been tested in overseas laboratory and plantation studies, sometimes of only one rust biotype against a limited range of host genotypes, provenances or seedlots, and provide only limited guidance for understanding wild spread of the rust in Australia. Large differences in resistance have been observed within and between species and between seedlots of the same provenance (Booth et al. 2000; Tommerup et al. 2003; Xavier et al. 2007), and intraspecific variability of hosts in disease reaction may be an important factor in determining the severity and impact of the disease as it naturalises and spreads in Australia (J. Walker in litt. Nov. 2010). Host species or genotypes with low disease severity may nevertheless act as reservoirs of the rust organism and support its spread (Zuaza et al. 2010b). A major resistance gene in one land-race of Eucalyptus grandis has been identified and mapped by Junghans et al. (2003), who note however that other secondary genetic factors (as well as rust biotype) are also involved in resistance; other samples of E. grandis have been shown to be susceptible in overseas situations and infection with the Myrtle Rust variant has been demonstrated in Australia under laboratory conditions (L. Morin in litt. March 2011). Rust variants may have different degrees of virulence, and different effects on hosts with which they have co-evolved compared with ‘naive’ hosts with no history of co-evolution (Tommerup et al. 2003). Only a few Australian taxa, each represented by few clones or seedlots, were found to be consistently resistant or apparently immune to infection by a limited range of rust biotypes under test conditions (Zuaza et al. 2010b): these are Austromyrtus tenuifolia, Corymbia tessellaris (Carbeen, Moreton Bay Ash), Corymbia calophylla var. rosea (a hybrid of C. calophylla and C. ficifolia), Gossia fragrantissima (Sweet Myrtle), Lophostemon confertus (Brush Box), Melaleuca ericifolia (Swamp Paperbark), Syzygium wilsonii subsp. cryptophlebium (Powderpuff Lilly Pilly), and Syzygium australe (Brush Cherry). The reported resistance of Corymbia tessellaris and Syzygium australe is however contraindicated by their confirmed infection with the Myrtle Rust variant in Australian tests. To the possibly resistant list, Plant Health Australia (2009) adds: Asteromyrtus magnifica and Lophostemon suaveolens.
21. Non-Australian species of Myrtaceae known to be susceptible to P. psidii sens. lat. (rust variants not documented) occur in the genera Acca (Feijoa), Campomanesia, Eugenia, Heteropyxis, Marlierea, Metrosideros, Myrcia, Myrcianthes, Myrciaria, Myrtus, Pimenta, Psidium, and Syzygium (Simpson et al. 2006; Zuaza et al. 2010b).
22. Australian native plant species currently known to be (variably) susceptible to infection by Puccinia psidii sens. lat. from testing overseas prior to April 2010, include species listed in the table below (Simpson et al. 2006; Plant Health Australia 2009; Zuaza et al. 2010b). The results of additional laboratory tests in Australia using the U. rangelii biotype are detailed in Point 9.
NSW, Qld, Vic
Qld, naturalised in NSW
Large-leaved Cabbage Gum
NSW, Qld, Vic
NSW, Qld, Vic
Eucalyptus amplifolia subsp. amplifolia
New England Blackbutt
Bangalay, Southern Mahogany
Cape York Red Gum
Eucalyptus camaldulensis subsp. simulata
Eucalyptus camaldulensis var. obtusa
River Red Gum
NSW, Qld, NT, WA
Eucalyptus globulus subsp. globulus
Tasmanian Blue Gum
Eucalyptus eugenoides (as ‘Eucalyptus nigra’)
NSW, Qld, Vic, Tas, SA
Large-fruited Red Mahogany
Sydney Blue Gum
Eucalyptus scias subsp. scias
Large-fruited Red Mahogany
NSW, Vic, Tas
Forest Red Gum
NSW, Qld, Vic
Qld, NT, WA
Eucalyptus tindaliae (incl. ‘Eucalyptus phaeotricha’)
NSW , Qld
Eucalyptus viminalis subsp. viminalis
NSW, Qld, Vic, Tas, SA
NSW, Qld, Vic, SA
NSW Vic Tas SA
A much larger number of taxa are likely to be susceptible.
Threatened entities and ecological processes at risk in New South Wales
23. As at March 2011, 74 species of plants belonging to the family Myrtaceae are listed as Threatened on the schedules of the NSW Threatened Species Conservation Act 1995: two species (both eucalypts) are listed as Critically Endangered, 27 species (12 eucalypts and 15 non-eucalypts) are listed as Endangered, and 45 species (30:15) are listed as Vulnerable. As yet, the susceptibility of these species to any exotic myrtaceous rust is unknown. The myrtaceous species listed under the Act are as follows (*asterisk indicates listing also under the Commonwealth Environment Protection and Biodiversity Conservation Act 1999):
CRITICALLY ENDANGERED SPECIES:
Babingtonia prominens [now = Kardomia prominens]
Babingtonia silvestris [now = Kardomia silvestris]
*Eucalyptus pachycalyx subsp. banyabba
Eucalyptus sp. Cattai (NSW 318983)
*Eucalyptus sp. Howes Swamp Creek (M. Doherty 19/7/85, NSW 207054)
*Babingtonia granitica [now = Kardomia granitica]
*Eucalyptus alligatrix subsp. miscella
*Eucalyptus caleyi subsp. ovendenii
Eucalyptus leucoxylon subsp. pruinosa
*Eucalyptus parramattensis subsp. decadens
*Eucalyptus robertsonii subsp. hemisphaerica
*Eucalyptus rubida subsp. barbigerorum
Melaleuca sp. Megalong Valley (Craven, Mallison & Douglas 10442)
24. As at March 2011, five Endangered Populations of myrtaceous species are listed on the schedules of the NSW Threatened Species Conservation Act 1995. Four are eucalypts (Eucalyptus camaldulensis population in the Hunter Catchment; population of Eucalyptus oblonga at Bateau Bay, Forresters Beach and Tumbi Umbi in the Wyong local government area; Eucalyptus parramattensis C. Hall subsp. parramattensis population in Wyong and Lake Macquarie local government areas; and Eucalyptus seeana population in the Greater Taree local government area). One listed Endangered Population is of a non-eucalypt: Darwinia fascicularis subsp. oligantha population in the Baulkham Hills and Hornsby Local Government Areas. All are within the projected high risk area for Eucalypt/Guava Rust, and within or relatively close to the existing (March 2011) distribution of the Myrtle Rust variant.
25. Most of the 98 threatened Ecological Communities listed on the schedules of the NSW Threatened Species Conservation Act 1995 (seven Critically Endangered, 88 Endangered, and three Vulnerable) have at least some species of Myrtaceae among the characteristic or ecologically ‘important’ constituents, and a majority of the listed ecological communities have eucalypts as dominant floristic and/or structural components.
26. Several of the plant species so far confirmed overseas as susceptible to P. psidii sens. lat. rust infection, but not listed under the Act, are structurally or floristically important in one or more ecological communities that are listed under the Act and that occur in the high-risk area of the State. These species include but are not limited to: Angophora costata, Corymbia gummifera, Eucalyptus botryoides, E. grandis, E. molluccana, E. paniculata, E. pilularis, E. robusta, E. saligna, E. tereticornis, and Syncarpia glomulifera.
27. The threat to Australia’s native biodiversity from introduced pathogens, including Rust Fungi of the order Pucciniales pathogenic on plants of the family Myrtaceae, may interact synergistically and unpredictably with other threat processes, and may cause species not currently regarded as Threatened to become so. Eagling (2007) notes that “the vulnerability of Australia to climate change is measurably increased by the invasion of exotic animal and plant species and vice versa.” ‘Anthropogenic Climate Change’ is listed as a Key Threatening Process under the NSW Threatened Species Conservation Act 1995. Interactions between the effects of rust epidemics and fire regimes are likely to be complex and case-specific as regards changes to fire frequency and severity, and for the effects of fire in locally reducing innoculum levels or promoting rust-susceptible flushes of new growth (Glen et al. 2007).
28. Puccinia psidii sens. lat. (Eucalypt/Guava Rust) “is regarded as one of the most serious threats to Australian production forests and natural ecosystems” (Commonwealth of Australia 2006). It has a potential to cause direct mortality in the estimated 10% of all Australian native forest plant species (and the great majority of dominant species) that belong to the family Myrtaceae, and with indirect effects that may include habitat loss for native fauna and flora, retarded regeneration and recruitment of younger trees and successional species, greater impact of fire, and abiotic effects as a result of canopy decline including erosion, reduced water quality, reduced water retention in soil and vegetation and potentially large losses through lost production to the forestry industry (Commonwealth of Australia 2006).
‘Introduction and establishment of Exotic Rust Fungi of the order Pucciniales pathogenic on plants of the family Myrtaceae’ is eligible to be listed as a Key Threatening Process as, in the opinion of the Scientific Committee:
it adversely affects threatened species, populations or ecological communities, or
could cause species, populations or ecological communities that are not threatened to become threatened.
Dr Richard Major
Proposed Gazettal date: 15/04/11
Exhibition period: 15/04/11 – 10/06/11
Aparecido CC, Figueiredo MB, Furtado EL (2003) Grupos de variabilidade fisiologica em populaces de Puccinia psidii. Summa Phytopathologica 29, 234-238
ANBG (2010) Australian flora & vegetation statistics. Australian National Botanic Gardens website: www.anbg.gov.au/aust-veg/australian-flora-statistics.html , accessed 10 August 2010.
APPS (2010a) ‘Puccinia psidii Winter – Pathogen of the Month, May 2010’. Australasian Plant Pathology Society website: www.australasianplantpathologysociety.org.au/Regions/POTM/index.htm , accessed 10 August 2010.
APPS (2010b) Guava Rust – by any other name, may be just as bad: Australia needs to do more now. [Media release, undated but c. June 2010, by the Australasian Plant Pathology Society. Available at: http://www.australasianplantpathologysociety.org.au/Press_Releases/index.html , accessed 12 August 2010.
Booth TH, Old KM, Jovanovic T (2000) A preliminary assessment of high risk areas for Puccinia psidii (Eucalyptus Rust) in the Neotropics and Australia. Agriculture Ecosystems and Environment 82, 295-301
Carnegie AJ, Lidbetter JR, Walker J, Horwood MA, Tesoriero L, Glen M, Priest MJ (2010) Uredo rangelii, a taxon in the guava rust complex, newly recorded on Myrtaceae in Australia. Australasian Plant Pathology 39, 463-466
de Carvalho AO, Alfenas AC, Maffia LA, do Carmo MGF (1994) Avaliacao do progresso da ferrugem (Puccinia psidii) em brotacoes de Eucalyptus cloeziana no sudeste da Bahia, de 1987 a 1989. Revista Arvore 18, 265-274
Commonwealth of Australia (2006) Contingency planning for Eucalyptus Rust. In ‘Records and Resolutions of the Primary Industries Ministerial Council’ [PIMC 10, 20 April 2006]: 100-104. (Available at: www.mincos.gov.au/publications#meeting_records ,
accessed 9 August 2010.
DAFF (2010) Questions and answers – Myrtle Rust. Commonwealth Department of Agriculture, Fisheries and Forestry. Available at: www.daff.gov.au/_data/assets/pdf_file/0009/1761372/myrtle-rust-qa.pdf, accessed 30 November 2010.
Eagling D (2007) Australian trade in agricultural food products – the challenge for plant pathologists. Australasian Plant Pathology 36, 539-542
Glen M, Alfenas AC, Zuaza EAV, Wingfield MJ, Mohammed C (2007) Puccinia psidii: a threat to the Australian environment and economy – a review. Australasian Plant Pathology 36, 1-16
Grgurinovic CA, Walsh D, Macbeth F (2006) Eucalyptus rust caused by Puccinia psidii and the threat it poses to Australia. EPPO Bulletin 36, 486–489
IPPC (2010) Myrtle Rust in Australia. Official Pest Report AUS-37/1 (04-05-2010). International Plant Protection Convention website. Available at: www.ippc.int accessed 20 August 2010.
Junghans DT, Alfenas AC, Brommonshenkel SH, Oda S, Mello EJ, Grattapaglia D (2003) Resistance to rust (Puccinia psidii Winter) in Eucalyptus: mode of inheritance and mapping of a major gene with RAPD markers. Theoretical and Applied Genetics 108, 175-180.
Killgore EM, Heu RA (2005) Ohia Rust Puccinia psidii Winter. State of Hawaii, Department of Agriculture, New Pest Advisory no 05-04 (updated December 2007). Available at: http://hawaii.gov/hdoa/pi/ppc/npa-1/npa05-04-ohiarust.pdf accessed 13 August 2010.
Langrell SRH, Tommerup IC, Zuaza EAV, Alfenas AC (2003) PCR based detection of Puccinia psidii from contaminated Eucalyptus germplasm – implications for global biosecurity and safeguarding commercial resources. In ‘8th International Congress of Plant Pathology’: 57
Langrell SRH, Glen M, Alfenas AC (2008) Molecular diagnosis of Puccinia psidii (guava rust) – a quarantine threat to Australian eucalypt and Myrtaceae biodiversity. Plant Pathology 57, 687-701
Loope L (2010) A summary of information on the rust Puccinia psidii Winter (guava rust) with emphasis on means to prevent introduction of additional strains to Hawaii: U.S. Geological Survey Open-File Report 2010-1082.
NSW Industry & Investment (2010a) PRIMEFACT 1017 (June 2010): Myrtle rust - Uredo rangelii. Available at: www.dpi.nsw.gov.au/biosecurity/plant/myrtle-rust/uredo-rangelii accessed 12 August 2010.
NSW Industry & Investment (2010b) ID-sheet: Identification of Myrtle rust (Uredo rangelii), July 2010. Available at: www.dpi.nsw.gov.au/__data/assets/pdf_file/0009/337374/identification-myrtle-rust.pdf accessed 12 August 2010.
Plant Health Australia (2007) National Plantation Timber Industry Biosecurity Plan. Plant Health Australia, Deakin ACT. Available at: www.planthealthaustralia.com.au/go/phau/biosecurity/plantation-timber accessed 17 August 2010.
Plant Health Australia (2008) National Nursery and Garden Industry Biosecurity Plan Version 2 (March 2008). Plant Health Australia, Deakin ACT. Available at: www.ngia.com.au [select ‘Environment’ then ‘Biosecurity’], accessed 10 August 2010.
Plant Health Australia (2009) Threat Specific Contingency Plan – Guava (eucalyptus) rust Puccinia psidii. Industry biosecurity plan for the nursery and garden industry. Plant Health Australia, Deakin ACT. (Available at: www.planthealthaustralia.com.au/go/biosecurity [select ‘Plant Information Document Database’, then ‘Nursery and Garden Industry’], accessed 9 August 2010.
Plant Health Australia (undated) Fact sheet: Exotic threats of plantation timber: Eucalyptus Rust. Available at: www.planthealthaustralia.com.au accessed 11 August 2010.
Ruiz RAR, Alfenas AC, Ferriera FA (1989) Influencia da temperatura, luz e origem do inoculo sobre a producao de uredosporos e teliosporos de Puccinia psidii. [Effect of temperature, light and inoculum source on urediniospore and teliospore production of Puccinia psidii.] Fitopathologia Brasileira 14, 70-73
Simpson JA, Thomas K, Grgurinovic CA (2006) Uredinales species pathogenic on species of Myrtaceae. Australasian Plant Pathology 35: 549-562
Tommerup IC, Alfenas AC, Old KM (2003) Guava rust in Brazil – a threat to Eucalyptus and other Myrtaceae. New Zealand Journal of Forestry Science 33, 420-428
Uchida J, Zhong S, Killgore E (2006) First Report of a Rust Disease on Ohia Caused by Puccinia psidii in Hawaii. Plant Disease 90, 524. Abstract available at: http://apsjournals.apsnet.org/doi/abs/10.1094/PD-90-0524C accessed 13 August 2010.
Uchida JY, Loope LL (2009) A Recurrent Epiphytotic of Guava Rust on Rose Apple, Syzygium jambos, in Hawaii. Plant Disease 93, 429. Available at:http://apsjournals.apsnet.org/doi/abs/10.1094/PDIS-93-4-0429B accessed 10August 2010.
Walker J (1983) Pacific mycogeography: deficiencies and irregularities in the distribution of plant parasitic fungi. Australian Journal of Botany, Supplementary Series 10: 89-136
Wilson PG, O’Brien MM, Heslewood MM, Quinn CJ (2005) Relationships within Myrtaceae sensu lato based on a matK phylogeny. Plant Systematics and Evolution 251, 3-19
Xavier, AA; von Sanfuentes E, Junghans DT, Alfenas AC (2007) Resistance of Eucalyptus globulus and E. nitens to rust. Revista Arvore 31(4): 731-735. English abstract and Portugese full text available at: http://www.scielo.br/ accessed 17 August 2010.
Zuaza EAV, Couto MMF, Lana VM, Maffia LA (2010a) Vertical spread of Puccinia psidii urediniospores and development of eucalyptus rust at different heights. Australasian Plant Pathology 39, 141-145
Zuaza EAV, Couto MMF, Lana VM, Maffia LA (2010b) Myrtaceae species resistance to rust caused by Puccinia psidii. Australasian Plant Pathology 39, 406-411
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