Ōhi‘a rust, also called guava rust in Brazil, myrtle rust, or Puccinia rust (Austropuccinia psidii (G. Winter) Beenken), formerly Puccinia psidii Winter) is a rust apparently native to parts of the American tropics. Rusts are a group of pathogenic fungi within the order Pucciniales. Ōhi‘a rust 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).
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 August 2007, the Hawaiian Department of Agriculture adopted an emergency rule banning importation of plants in the myrtle family from “infested areas,” specified as South America, Florida, and California. This rule expired in August 2008. A permanent rule which banned all imports of plants in the Myrtaceae except by permit and under certain conditions was drafted in 2015 and approved by the Hawai‘i Board of Agriculture but has not yet been adopted. Meanwhile, USDA APHIS official have reiterated that the agency considers Austropuccinia psidii a non-actionable, non-reportable pest, and therefore it would not be kept out of Hawai`i if intercepted at the border coming from a foreign country. To change that APHIS verdict, HDOA needs to demonstrate that multiple strains or races of A. psidii exist and that there is no practical way of distinguishing new, potentially more virulent, strains from the one already present in Hawai`i (Loope 2009). Discussions on the rule continue and the Hawaii Dept. of Agriculture hopes that the rule will be adopted in 2018.
Currently, Hawai`i relies on visual inspection – a less than ideal approach since both limited inspection capacity and the high likelihood of some infections being latent (asymptomatic) at the time material is shipped constrain the ability to detect the rust. New molecular tests could improve detection efficiency, but cost and the time required to process samples preclude routine use (Loope 2009).
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.
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.
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
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
Killgore, E. M. and R. A. Heu. Ohia rust, Puccinia psidii Winter. Hawaii Department of Agriculture New Pest Advisory No. 05-04 December 2007. URL: http://hdoa.hawaii.gov/pi/files/2013/01/npa05-04-ohiarust.pdf
Loope, L. and A.M. LaRosa. 2008 ‘Ohi’a Rust (Eucalyptus Rust) (Puccinia psidii Winter) Risk Assessment for Hawai`i
Loope, L. 2009. A summary of Information Related to Regulatory Options for Preventing Introduction of Additional Strains of the Rust Puccinia psidii Winter (Guava Rust) To Hawaii
Stewart, J. E., A. L. Ross-Davis, R. N. Graça, A. C. Alfenas, T. L. Peever, J. W. Hanna, J. Y. Uchida, R. D. Hauff, C. Y. Kadooka, M.-S. Kim, P. G. Cannon, S. Namba, S. Simeto, C. A. Pérez, M. B. Rayamajhi, D. J. Lodge, M. Agruedas, R. Medel-Ortiz, M. A. López-Ramirez, P. Tennant, M. Glen, P. S. Machado, A. R. McTaggart, A. J. Carnegie, and N. B. Klopfenstein. 2018. Genetic diversity of the myrtle rust pathogen (Austropuccinia psidii) in the Americas and Hawaii: Global implications for invasive threat assessments. Forest Pathology 48(1): 1-13. https://doi.org/10.1111/efp.12378