- Introduced to 27 countries on several continents; most worrying has been the spread across the Pacific beginning after 2000.
- Known to infect 539 species worldwide from 86 different genera – all in the Myrtaceae family. Some are killed, others survive; some hosts support spread of the infection. The IUCN Red list already includes 338 species in the family – before determining impacts of the rust (CABI)
- The Myrtaceae family is particularly prominent in Australia, New Zealand, and other forested areas associated with the former supercontinent of Gondwanaland. Host species and genera include the dominant tree genera in Hawai`i (‘ōhi‘a) Oceania (Eucalyptus, Melaleuca, …). Eucalyptus is widely used in forestry around the world.
- One principal pathway of introduction is imports of infected plants or plant parts. Other possible pathways include timber and wind.
- Four biotypes are known. The “pandemic” biotype introduced to Oceania, Asia and the Pacific, including Hawai`i, Australia, New Zealand, New Caledonia, and Florida. This biotype is not known to be present in Brazil. A distinct biotype has been introduced to South Africa (Toome-Heller et al. 2020).
Ōhi‘a rust, also called myrtle rust, eucalyptus rust or guava rust, is a rust apparently native to parts of the American tropics. It was first described on guava (Psidium pomiferum) in Brazil in 1884 (Loope and La Rosa 2008). Austropuccinia psidii is unusual among rusts in having a wide host range. Of the nearly 6,000 plant species (in about 132 genera) in the family Myrtaceae, more than 520 species in 70 genera (or 9% of species, 53% of the genera) worldwide are known to be hosts [Geoff Pegg, Australian workshop].
The rust experienced a rapid dispersal after 2000. It was detected in Hawai`i in 2005, Japan in 2007, China in 2009, Australia in 2010, New Caledonia and South Africa 2013, Indonesia and Singapore in 2016, and New Zealand in 2017.
Ōhi‘a rust in Hawai‘i
Austropuccinia psidii was detected in Hawai‘i during spring 2005. The rust spread rapidly — by August 2005 it had been found throughout the main Hawaiian Islands (Loope and La Rosa 2008). The rust has infected six native plant species and at least 24 non-native species (Anderson 2012). The endangered endemic plant Eugenia koolauensis has been devastated; it is now reproducing only in nurseries where it can be treated for the fungus (J. B. Friday). Also attacked is the non-endangered indigenous species Eugenia reinwardtiana (Loope 2009). The native tree ‘ōhi‘a (Metrosideros polymorpha) has largely escaped major damage. Most affected has been the widespread invasive plant rose apple (Syzygium jambos).
The rapid spread of ‘ohi‘a or myrtle rust after its introduction was probably driven by high rates of infection and mortality in the invasive rose apple (Syzygium malaccense). Now, after collapse of rose apple populations, Austropuccinia infections are probably maintained at low to moderate levels in ‘ohi‘a and non-native Myrtaceae species (Atkinson and Roy, 2023).
‘Ōhi‘a rust threatens other native Hawaiian species, especially the federally-listed Eugenia koolauensis. While mortality of ‘ohi‘a has been low to date, approximately 5% of trees are infested, with with from 5 to 10% of leaves carrying the fungus. Recent outbreaks on O`ahu, with defoliation and mortality, has heightened concern about impacts of the disease (Atkinson and Roy, 2023).
Because of concern that introduction of a new strain of the ‘ohi‘a rust fungus might lead to higher levels of disease, Atkinson and Roy (2023) tested use of a network of passive environmental samplers to detect the pathogen’s presence through measuring airborne environmental DNA (eDNA). They found that simple equipment is an effective method to monitor airborne spread of Austropuccinia psidii when combined with sensitive molecular detection methods. This monitoring would be helpful in detecting introduction of any new strains or in selecting sites for planting endangered Eugenia koolauensis as part of restoration efforts.
Atkinson and Roy’s (2023) findings also provide additional information about the pathogen’s varying levels. Detections of Austropuccinia spores was highest in the spring (March–May) and fall (September–November); lowest in summer (June–August). This might be related to seasonal flushes of new growth in ‘ohi‘a, or to summer declines in rainfall and humidity. They also found regional differences – some of them puzzling. While the wet, cool montane northern Kohala mountains supported the highest number of spores detected (100% of samples), an area with very similar rainfall, temperature, humidity, and elevation characteristics, the Kilauea Crater area had the lowest numbers detected (3 to 14% of samples). Atkinson and Roy (2023) speculate that this difference might be caused by lower infection rates in ‘ohi‘a at Kilauea Crater, differences in abundance of potential (introduced) secondary hosts for the rust, or differences in other environmental factors that can affect germination of spores.
Any threat to ‘ōhi‘a would be alarming because these trees overwhelmingly dominate approximately 80% of Hawai`i’s remaining native forest. A persistent, severe infestation of Austropuccinia rust that destroys new growth on ‘ohi’a trees causes crown dieback, and, eventually, death of the mature trees. Loss of ‘ōhi‘a could result in significant changes to the structure, composition, and potentially, the function, of forests on a landscape level. ‘Ohi’a forests are home to the Islands’ one native terrestrial mammal (Hawaiian hoary bat) and 30 species of forest birds – especially the unique honeycreeper endemic subfamily. Eighteen of 19 extant Hawaiian honeycreepers in the main Hawaiian islands, including 12 of 13 species listed as endangered by the U.S. Fish and Wildlife Service, depend on ‘ōhi‘a for critical habitat (Loope and LaRosa 2008). Increased light reaching the forest floor following canopy dieback would increase the likelihood of invasion by light-loving non-native species, of which Hawai`i has dozens. Loss of ‘ōhi‘a would thus also damage habitat for one-third to one-half of Hawai`i’s approximately 300 endangered plant species (Loope and LaRosa, 2008) through encouraging non-native competitors and changing understory environmental conditions.
‘Ōhi‘a also has significant cultural values to the Hawaiian people through its connection to the deities Ku, Pele (volcanoes) and Laka (hula) (Loope and LaRosa, 2008).
Conservationists and authorities have prioritized preventing the introduction of new strains that might be either more virulent or more cold-tolerant and thus able to damage forests at higher elevations. Research in the pathogen’s native range in Brazil (funded by the USDA Forest Service) has demonstrated the presence of other strains of Austropuccinia that are much more virulent on ‘ōhi‘a than the type now present in Hawai‘i (Costa da Silva et al. 2014). An analysis of the genetics of Austropuccinia psidii (Stewart et al. 2018) revealed nine genetic clusters, with all samples from Hawai‘i and the Pacific belonging to two genetic clusters, which together make up one “pandemic biotype” that is associated with disease in Florida, Hawai‘i, and Oceania.
The most likely pathway by which Austropuccinia rust was introduced to the Hawaiian Islands was myrtle (Myrtus communis) foliage used in floral arrangements. Maui inspectors have intercepted the rust on myrtle from southern California several times in 2006 and 2007. (Loope 2009). The rust’s presence in California was reported in late 2005 (Mellano 2006, cited by Loope and LaRosa 2008). The same strain of the pathogen causing disease in Hawai`i is also found in California (Stewart et al. 2018).
Ōhi‘a rust in Florida
Florida is known to have multiple strains of Austropuccinia rust. Florida has eight native species of Myrtaceae that are also native further south in the Neotropics. Only one of those species, Myrcianthes fragrans, has been recorded as a host of the rust, and infection has apparently been minimal. (Loope and LaRosa 2008)
There is strong evidence of host specialization among the various strains of this pathogen, since the strain of the pathogen associated with one host plant species often does not infect other plant species known to be hosts (Loope 2009). For example, the strain (genotype) of the pathogen now in Hawai`i does not utilize many of the species known to be infected by the rust elsewhere, including common guava (a widespread invasive on the Islands) (Loope 2009). New Zealand scientists report that the South African strain can complete its life cycle more quickly on New Zealand hosts than can the “pandemic” strain currently established there [Julia Soewarto, AU workshop].
The presence of Austropuccinia psidii in Florida for at least 30 years (Loope 2009) greatly complicated the regulatory situation in the United States, since an organism that is already in the country cannot be treated as a “quarantine pest” unless there is an “official control program” targeting the pest.
In May 2020, the Hawaii Department of Agriculture adopted a rule restricting the import of plants in the Myrtaceae, including live plants and foliage used in cut flower arrangements. Dried, non-living plant parts, seeds that are surface sterilized, and plants in tissue culture in sterile media and containers are exempted from the ban. Other importations may be done by permit.
In 2019, the USDA Animal and Plant Health Inspection Service (APHIS) proposed to prohibit importation of plants for planting of all taxa in the Myrtaceae family when those imports are destined for Hawai`i. This action was carried out under the agency’s authority to prohibit temporarily importation of certain taxa of plants for planting as not authorized for importation pending pest risk assessment (NAPPRA). This action is proposed with the aim of reducing the probability of introduction of additional strains of Austropuccinia psidii. The proposed quarantine applied to shipments to Hawai`i only. The proposed action has not yet taken effect.
Although import of foliage and live plants in the Myrtaceae to Hawai`i is now banned, accidental or deliberate smuggling of plants or plant parts remains a threat. Because there are thousands of species in the family, agricultural inspectors might not be able to identify plants or foliage if included in a shipment. The source material could originate from the pathogen’s native range in South America or from any of the many places to which the pathogen has been introduced, including Central America, Florida, California, Oceania, or various countries in Asia.
CABI recognizes several possible pathways:
- infected or contaminated planting material, nursery stock, plant cuttings, flowers and germplasm
- contaminated plant waste, timber, wood packaging and dunnage
- contaminated equipment and tools used on or around plants (e.g. chainsaws, secateurs)
- contaminated clothing, shoes and other personal effects
Imports of wood packaging, logs, and lumber involving tropical hardwood species (including Eucalyptus) into Hawai`i must be debarked or fumigated (Code of Federal Regulations – 7 CFR 319.40-5). Until the NAPPRA proposal is finalized, imports to the United States of most living plants are subject only to inspection (Code of Federal Regulations – 7 CFR319.37). The tiny size of the rust spores makes detection during inspection unlikely unless the plant is displaying symptoms of the disease.
Ōhi‘a rust in Australia and New Zealand
Myrtle rust was detected in Australia in 2010, New Caledonia in 2013 and New Zealand in 2017. The introductory pathway to Australia has never been identified. The rust is believed to have been carried to New Caledonia and New Zealand by wind from Australia across the Tasman Sea. The strain of the pathogen present in all these areas is the same strain as in Asia and Hawai`i (Beresford et al. 2019). (A separate strain of the pathogen has been introduced to South Africa; Toome-Heller et al. 2020)
These areas are particularly vulnerable to myrtle rust. Australia is floristically dominated by Myrtaceae. Approximately 2,250 Myrtaceous species in 88 genera grow across the continent. This equates to 38% of all species in the Myrtaceae globally, 66% of the genera. Myrtaceae occur in 11 of 13 major vegetation formations. Eucalypt forests make up 74% of Australia’s forested area. Trees and shrubs in the Myrtaceae provide essential habitat, nectar & pollen for vertebrates & invertebrates; fleshy fruits eaten by birds & mammals; hollows for cavity nesters; and support diverse microbial communities [Brett Summerell, Australian workshop].
As of spring 2021, 382 of Australia’s Myrtaceae species – in 57 genera – are known to host the rust. Thus, 7% of Australia’s 2,253 known native Myrtaceae are already known to be vulnerable to some extent [Brett Summerell, Australian workshop]; scientists expect more host species to be identified. Hosts include species in the Eucalyptus, Melaleuca and Leptospermum genera (Carnegie et al. 2016). Forty-three of the species (11% of the known hosts) are severely affected [Brett Summerell, AU workshop]. Three species have been officially listed as critically endangered – Rhodamnia rubescens and Rhodomyrtus psidioides are formerly widespread understory trees in rainforests; Lenwebbia sp. is narrowly endemic, growing in stunted cloud forests on clifftops in a single mountain range. For a detailed analysis of the impacts of A. psidii on Rhodamnia rubescens and Rhodomyrtus psidioides in New South Wales, see Winzer et al. (2020). Experts predict extinction of additional rainforest species within a generation; one study placed 16 species in this category. (For comparison, only 12 plant species in Australia have become extinct since arrival of the first Europeans 200 years ago. [Julian Radford-Smith, Australian workshop]). In Queensland, 48 species are highly or extremely susceptible (Carnegie and Pegg (2018). Entire ecosystems are at risk: no other tree species can replace the Melaleuca genus’ tolerance of standing water. [Bob Makinson, Australian workshop] A detailed discussion of impacts on plant communities to date is provided by Carnegie and Pegg (2018).
Originally the pathogen was spread by human activities, especially movement of plants. As it became more widespread, windborne spread of spores has become important. As of spring 2021, myrtle rust is widespread and well established in a range of native ecosystems in the eastern mainland states of New South Wales and Queensland and part of the Northern Territory. The disease has been detected in Victoria and Tasmania but impact is limited to urban gardens. It has not yet been detected in South or Western Australia.
After an initial eradication effort failed, the federal government apparently stepped back. A proposal to list myrtle rust as a Key Threatening Process https://www.environment.gov.au/biodiversity/threatened/key-threatening-processes or at the federal level failed (Carnegie et al. 2016). Some scientists point to this decision and the availability of funding to study only species already listed as endangered as barriers to more pro-active management of the disease’ impact. [Craig Stehn and Bob Makinson, Australian workshop] Australia has prohibited movement of plants and other commodities to South Australia and West Australia. The Australian government also funds seed collection and other ex situ conservation efforts. But little funding has been available even for impact studies. [Australian workshop]
In 2018 a scientist affiliated with the Australian Network for Plant Conservation published a draft conservation plan. https://www.apbsf.org.au/wp-content/uploads/2018/06/Myrtle-rust-action-plan_accessible.pdf Plan development had input from staff at the Plant Biosecurity Cooperative Research Centre and the Australian Government Department of the Environment and Energy. The goal was to help direct and stimulate further research on critical questions and build awareness of the potentially devastating effects myrtle rust might have if it remains unchecked. As of April 2020, no funding had yet become available to finalize and implement the report (Dr. Michael Robinson, Managing Director, Plant Biosecurity Science Foundation).
A detailed discussion of Australia’s response to the rust invasion is provided by Carnegie and Pegg (2018).
In 2018, the state of New South Wales adopted a strategy based on the NGO conservation plan. The state began funding the “Saving our Species” Myrtle Rust program in 2019. Much of NSW effort has been focused on documenting the rapid decline of two of the endangered species, Rhodamnia rubescens and Rhodomyrtus psidioides; and promoting ex situ conservation efforts for these species.
New Zealand is almost as vulnerable. These islands are home to 27 – 30 native plants in Myrtaceae family (Bereford et al. 2019). Twenty-four species and six hybrids have been confirmed to be naturally infected by myrtle rust in New Zealand. Thirteen of the hosts are exotic species (Toome-Heller et al. 2020). When myrtle rust was first detected, starting May 2017, the Ministry of Primary Industries and Department of Conservation surveyed Myrtaceae across natural and urban areas. By April 2018, the pathogen had been detected in 12 mainland regions, including most of the North Island and north-western parts of the South Island. At that time, the government changed its program to focus on long-term management and the frequency of surveillance updates decreased (Bereford et al. 2019). A climate analysis determined that the northern half of the North Island and northwest district of the South Island (Tasman District).
The myrtle rust detection in New Zealand coincided with the seasonal mass distribution of myrtaceous plants from commercial nurseries to planting programs. Many plants were moved long distances before controls were established (Toome-Heller et al. 2020). Nurseries are reported now to be careful to produce Myrtaceae plants that are rust-free [Beccy Ganley AU workshop].
Vulnerability of some species remains unclear because environmental conditions apparently play an important role in disease progression. However, at least one species – Lophomyrtus – is not reproducing. Scientists have detected 109 species of birds, invertebrates, vascular plants (mistletoe), and fungi associated with this shrub. Concern about economic impacts focuses on Leptospermum scoparium, which is utilized in production of manuka honey. [AU workshop] Scientists have determined that the unique biotype of A. psidii found in South Africa can complete its lifecycle more quickly on New Zealand native plants than can the “pandemic” strain [Julia Soewarto, AU workshop]
The New Zealand government continues to support research, although it is no longer monitoring spread of the rust [Roanne Sutherland and Beccy Ganley AU workshop]. Stakeholders in New Zealand appear to be much more concerned about myrtle rust than their counterparts in Australia (Toome-Heller et al. 2020). See the research plan and reports of results to date at https://www.fisheries.govt.nz/dmsdocument/37290/direct
The island of New Caledonia – an overseas territory of France in the Coral Sea East of Australia – has 250 Myrtaceae species in 26 genera. Of these, 99% are endemic. At least 67 of these species – all endemics – are known to host the rust. It is probable that more species are vulnerable. [Julia Soewarto, AU workshop]
Southern Africa also has at least 24 native plants in the Myrtaceae. All but one grow in forests or grasslands along the Indian Ocean Coastline of South Africa — in Kwazulu-Natal and Mpumalanga to Limpopo and into Mozambique. Some species of Heteropyxis and Syzygium are found farther inland in savannah areas of Limpopo, Mpumalanga, North West and Gauteng, into Botswana, Zimbabwe and further north in tropical Africa. One species, Metrosideros angustifolia, is confined to the Cape Floristic Region in the western part of the country. [Braam van Wyk pers. comm.]
South Africa relies heavily on plantations of Eucalyptus, some species of which might be vulnerable to the various biotypes of the rust.
As noted above, the biotype detected in South Africa 2013 is unique.
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