Ōhi’a (Austropuccinia) Rust

ohi'a rust on a leaf
Austropuccinia psidii
(G. Winter) Beenken (formerly Puccinia psidii Winter)
J.B. Friday and Faith Campbell

Ōhi‘a rust, also called myrtle rust, guava rust in Brazil, or Puccinia rust (Austropuccinia psidii (G. Winter) Beenken), formerly Puccinia psidii Winter) 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, which is believed, so far, to include all the species in the family Myrtaceae. More than 450 species have been identified as hosts (Stewart et al. 2018). The full host range of A. psidii is unknown (Loope 2009).

  • 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)
  • Host species and genera include the dominant tree in Hawai`i – ‘ōhi‘a; and Eucalyptus in native range of Australia but widely used in forestry around the world.
  • The Principal pathway of introduction is imports of infected plants or plant parts.
  • Two biotypes – pandemic biotype- in Asia & Pacific, including Hawai`i, Australia, New Zealand, and Florida – is not known to be present in BR. Separate biotype introduced to South Africa  (Toome-Heller et al. 2020);

Austropuccinia psidii was discovered in Hawai‘i during spring 2005, when authorities were alerted to an infected native ‘ōhi‘a (Metrosideros polymorpha) tree. 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).

In late 2017 an outbreak of Austropuccinia caused widespread defoliation and mortality of ‘ōhi‘a across hundreds of acres in at least four locations on windward O‘ahu and on Moloka‘i. It is unknown if a new, more virulent strain has been introduced to Hawai‘i or if a period of unusually wet weather precipitated the outbreak. The pathogen was not associated with widespread ‘ōhi‘a mortality on the other Hawaiian islands despite widespread presence of the rust on rose apple (Syzygium jambos), the preferred host.

The new outbreak is alarming because ‘ōhi‘a 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 are pressing for implementation of a strategy aimed at 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 has shown there are 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). A recent 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, Australia, and Indonesia.

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).

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).

The presence of Austropuccinia psidii in Florida for at least 30 years (Loope 2009) greatly complicates the regulatory situation, 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 part, 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.

Although import of foliage and live plants in the Myrtaceae 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 may not be able to identify plants or foliage if included in a shipment. Other possible pathways for movement of Austropuccinia rust are trade in live plants or wood products with bark. 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, Australia, 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

In 2019, the USDA Animal and Plant Health Inspection Service (APHIS) proposed to designate the importation of certain taxa of plants for planting as not authorized for importation pending pest risk assessment (NAPPRA) in order to prevent the introduction of quarantine pests into the United States. One of the taxa included in the proposal was all taxa of Myrtaceae family in order to reduce 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.

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). Imports 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.

Myrtle Rust in Australia and New Zealand 

Myrtle rust was detected in Australia in 2010, New Caledonia in 2013 and New Zealand in 2017. It is believed to have been carried to Australia and New Caledonia on imported plants or cut vegetation; to  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, with 393 native species from 52 genera. These include Eucalyptus, Melaleuca and Leptospermum (Carnegie et al. 2016). This equates to 40% of all species in the Myrtaceae globally, 60% of the genera (Winzer et al. 2020). At least 393 of these native species can be infected by myrtle rust (Winzer et al. 2019). 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 2020, myrtle rust is widespread in the eastern mainland states of New South Wales and Queensland; and has been detected in Victoria, Northern Territory and Tasmania. It has not yet been detected in South or Western Australia (Winzer et al. 2019).

After an initial eradication effort failed, the federal government has apparently stepped back. A proposal to list myrtle rust as a Key Threatening Process https://www.environment.gov.au/biodiversity/threatened/key-threatening-processes#:~:text=A%20process%20can%20be%20listed,conservation%20dependent%20category)%3B%20or at the federal level failed (Carnegie et al. 2016).  A group of scientists undertook the first studies on myrtle rust’s impact on native vegetation about nine years after the pathogen appeared. The studied two formerly widespread species that are not listed as critically endangered in New South Wales, Rhodamnia rubescens and Rhodomyrtus psidioides (Winzer et al. 2020). Their field experiment tested the direct and indirect effects resulting from the small trees’ infection. They found, inter alia, that in their study plots there were no adult R. psidioides. Seedlings were 190% less common. The second tree, R. rubescens, produced no viable seeds; there was a 112% reduction in seedlings. Increased canopy transparency of these trees — on average 19% greater canopy transparency – led to 8% lower species richness and 46% lower total abundance among understorey species overall. In other words, reproduction of these species had basically stopped. Furthermore, they found no recruitment of other Myrtaceae species, either.

In 2018 a scientist affiliated with the Australian Network for Plant Conservation published a draft conservation plan. http://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).

New Zealand is almost as vulnerable. These islands are home to 27 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 changes 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 NZ coincided with the seasonal mass distribution of myrtaceous plants from commercial nurseries to planting programmes. Many plants were moved long distances before controls were established (Toome-Heller et al. 2020).

Scientists in New Zealand have determined that A. psidii can overwinter as a latent infection without reproducing. A. psidii can reproduce sexually, although the importance of the sexual cycle in seasonal epidemic development is not yet understood (Bereford et al. 2019).

It is also notable that the unique biotype of A. psidii found in South Africa has already been found to be pathogenic towards some NZ native Myrtaceae  (Toome-Heller et al. 2020).

There continues to be confusion about the degree to which specific plant species are vulnerable. Results from field detections sometimes vary from laboratory tests. Scientists think environmental conditions play a significant role in whether a plant becomes diseased (Toome-Heller et al. 2020). Concern is especially high regarding Leptospermum scoparium, the plant utilized in production of manuka honey (Toome-Heller et al. 2020).

 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

 

Sources

Anderson, R. 2012. A baseline analysis of the distribution, host-range, and severity of the rust Puccinia psidii in the Hawaiian Islands, 2005 – 2010 . Technical Report HCSU-031. USGS, Honolulu, HI.

Beenken, L. 2017. Austropuccinia: a new genus name for the myrtle rust Puccinia psidii placed within the redefined family Sphaerophragmiaceae (Pucciniales). Phytotaxa 297(1): 53-61. DOI: 10.11646/phytotaxa.297.1.5

Beresford, R., G. Smith, B. Ganley and R. Campbell. 2019. Impacts of myrtle rust in NZ since its arrival in 2017. 2019. New Zealand Garden Journal 2019, Vo. 22 (2).  https://www.myrtlerust.org.nz/assets/news/NZ-Garden-Journal-Dec-2019-p5-10.pdf

CABI Austropuccinia psidii datasheet https://www.cabi.org/isc/datasheet/45846

Carnegie, A.J., A. Kathuria, G.S. Pegg, P. Entwistle, M. Nagel, F.R. Giblin. 2016. Impact of the invasive rust Puccinia psidii (myrtle rust) on native Myrtaceae in natural ecosystems in Australia. Biological Invasions (2016) 18:127–144

Code of Federal Regulations. January 1, 2005 (Title 7, Volume 5). 7 CFR319.40-5: Logs, lumber, and other unmanufactured wood articles – importation and entry requirements for specified articles. (available by using search engines/retrieval services at http://www.gpoaccess.gov/fr/index.html).

Code of Federal Regulations. January 1, 2005 (Title 7, Volume 5). 7 CFR319.37: Nursery stock, plants, roots, bulbs, seeds, and other plant products – prohibitions and restrictions on importation: disposal of articles refused importation. (available by using search engines/retrieval services at http://www.gpoaccess.gov/fr/index.html).

Costa da Silva, A; PM Teixeira de Andrade, A Couto Alfenas, R Neves Graca, P Cannon, R Hauff, D Cristiano Ferreira, and S Mori. 2014.  Virulence and Impact of Brazilian Strains of Puccinia psidii on Hawaiian Ohia (Metrosideros polymorpha). Pacific Science 68(1):47-56. doi: http://dx.doi.org/10.2984/68.1.4

Hawaii Administrative Rules, Chapter 4-70, Subchapter 15: Introduction of Myrtaceae. (https://hdoa.hawaii.gov/wp-content/uploads/2020/05/Subchapter-15-Introduction-of-Myrtaceae.pdf)

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United States Department of Agriculture Animal and Plant Health Inspection Service.  2019. Plants for Planting Whose Importation Is Not Authorized Pending Pest Risk Analysis; Notice of Availability of Data Sheets for Taxa of Plants for Planting That are Quarantine Pests or Hosts of Quarantine Pests https://www.federalregister.gov/documents/2019/11/25/2019-25439/plants-for-planting-whose-importation-is-not-authorized-pending-pest-risk-analysis-notice-of

Winzer, L.F., K.A. Berthon, A.J. Carnegie, G.S. Pegg, M.R. Leishman. 2019. Austropuccinia psidii on the move: survey based insights to its geographical distribution, host species, impacts and management in Australia. Biological Invasions April 2019, Volume 21, Issue 4, pp 1215–1225

Winzer, L.F., K.A. Berthon, P. Entwistle, A. Manea, N. Winzer, G.S. Pegg, A.J. Carnegie, M.R. Leishman. 2020. Direct and indirect community effects of the invasive plant pathogen Austropuccinia psidii (myrtle rust) in eastern Australian rainforests. Biological Invasions Volume 22, pages2357–2369 (2020)