Why such scattershot responses to myrtle rust?

Pacific countries’ policy and management responses to the spread of the myrtle rust pathogen, Austropuccinia psidii (formerly Puccinia psidii), has had puzzling – even infuriating – gaps … which perhaps have contributed to its spread and damage.

Reminder: ‘ōhi‘a or myrtle rust attacks species in the Myrtaceae – a family now said to include 5,600 species (Stewart et al. 2018). Ten percent of Australia’s native flora is in the family – or about 1,300 species. New Zealand is home to 27 native plants in the Myrtaceae family (Bereford et al. 2019) and the Hawaiian Islands to eight (JB Friday pers. comm.).  See a writeup about the disease here.

Austropuccinia psidii is one of the global invaders: it has invaded 27 countries on several continents. It is apparently native to parts of the American tropics.

Levels of worry rose considerably with the pathogen’s spread across the Pacific beginning with the detection in Hawai‘i in spring 2005. Additional introductions in the region were Japan in 2009; China in 2011; Australia, New Caledonia, and South Africa in 2013; and New Zealand in 2017.

The known host range currently exceeds 500 species in 86 genera – all in the Myrtaceae family. The pathogen has several strains or biotypes; the impact of the various biotypes on the various host species differs. Environmental factors also apparently affect disease.

[For my earlier discussions of threats to the unique Hawaiian flora, go here for dryland flora, here and here for more general discussions. I discuss National Park Service efforts – including in Hawai`i – here.]

There are several factors that militate against a political entity choosing to act:

1) Inherent Difficulty in Controlling Wind-Borne pathogen

In both Hawai`i and Australia, the rust spread rapidly once it was established outside of nurseries. In Hawai`i, it had spread to all the islands within a few months of its detection in spring 2005 (Loope and La Rosa 2008). In Australia, the rust was established in natural ecosystems throughout coastal New South Wales and to far northern Queensland by mid-2012 – less than two years after detection (Carnegie et al. 2016). The number of host species also expanded rapidly – from 214 native plants in 2016 (Carnegie et al. 2016) to 393 species by 2019 (Winzer et al. 2019). Myrtle rust is believed to have been carried to Australia and New Caledonia on imported plants or cut vegetation; then to New Zealand by winds from Australia across the Tasman Sea (Toome-Heller et al. 2020).

2) Lack of Clarity About Probable Impacts

Austropuccinia psidii had been introduced fairly widely before 2000, and some biotypes had caused significant damage on introduced species within both the native and introduced ranges of the rust – e.g., Eucalyptus in Brazil, allspice (Pimento doica) in Jamaica, rose apple (Syzygium jambos) in Hawai`i.  However, the rust had had little impact on native floras in introduced ranges, especially not on widespread species (Carnegie et al. 2016).

However, concerns existed in the Pacific region because of:

• Its wide host range (before the introduction to Australia, the known host range was “only” 129 species in 33 genera Carnegie et al. 2016).
• The severe damage to Australian genera growing outside their native range, e.g., nurseries and plantations of Eucalyptus in South America and Melaleuca quinquenervia and Rhodomyrtus tomentosa in Florida (Carnegie et al. 2016)

In Hawai`i, ‘ōhi‘a rust caused little damage to the dominant tree species in Hawaiian forests, ‘ōhi‘a lehua for the first 10 years after its introduction. The rust did cause severe damage to the invasive alien shrub rose apple and several native plants, especially the endangered Eugenia koolauensis. A more damaging outbreak in ‘ōhi‘a lehua trees in 2017 has increased concern.

So – while Austropuccinia psidii has an extremely wide host range, its impact in naïve ecosystems to which it might be introduced is unclear.

In most cases, lack of knowledge about a pest’s impacts on naïve hosts in new ranges is almost inevitable – unless scientists undertake host vulnerability tests. Such tests are rarely done in advance of an introduction. One exception is European scientists evaluating European trees’ vulnerability to a suite of newly discovered Phytophthora species in Vietnam and elsewhere.  (I am unaware that U.S. scientists are carrying out parallel studies.)

Still, environmental and other factors play important roles and might counter expectations raised by lab experiments or experience of hosts planted in non-native sites. In Australia, McRae (2013) noted that the “mycological firestorm” predicted by environmentalists to result from introduction of the rust had not occurred. This at least partly explained waning interest in combatting the pathogen (Carnegie et al. 2016).

In my view, the swings in perceptions of the risk reflected more flaws in understanding than actual risk. Impacts can take time to manifest – especially when, as with Austropuccinia psidii – the pathogen is known to affect primarily new growth and fruit and flowers (Carnegie et al. 2016). The impact might be greatest in the form of suppressing regeneration rather than by killing mature trees right away. [See beech leaf disease as another possible example of this phenomenon.]

Questions hampering predictions of impact were further confused by taxonomic questions (Carnegie et al. 2016). Austropuccinia psidii has at least nine genetically distinct clusters. So far, two have been introduced outside South/Central America. One strain – called the “pandemic biotype” – has been found at all introduction sites in Florida, Hawai‘i, Asia, and the Pacific – Australia, New Zealand, New Caledonia (Stewart et al. 2018). This biotype is not known to be present in Brazil (Toome-Heller et al. 2020). A second biotype has been introduced to South Africa; it has been shown to be able to infect some Myrtaceae in New Zealand (Toome-Heller et al. 2020). See especially Stewart et al. 2017, full citation below.

3) Policy Barriers Created by Phytosanitary Regulations

In the U.S., the pathogen has been established in one state – Florida – since 1977. There, it is not considered to be causing damage to important species. Under U.S. regulations – reflecting the international trade rules – 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. (For a discussion of this issue, see the analysis of the SPS Agreement in Chapter 3 and Appendix 3 of Fading Forests II). For this reason, when ‘ōhi‘a rust was detected in Hawai`i in 2005, USDA’s Animal and Plant Health Inspection Service (APHIS) was unable to adopt regulations governing imports or interstate movement of vectors (i.e., cuttings or nursery stock of plant species in the Myrtaceae).  

The State responded to the initial detection by adopting an emergency order two years later, in August 2007. This prohibited importation of plants in the myrtle family from “infested areas”- specified as South America, Florida, and California. This state rule expired in August 2008.

It became apparent that USDA APHIS would not take action to assist Hawai`i unless APHIS accepted  scientific findings as proving that additional biotypes of the rust existed that could pose a more severe threat to plants on the Islands. Such studies were undertaken, some funded by the USDA Forest Service.  This process took years. During this period, Hawai`i developed a permanent rule which was adopted in May 2020. This regulation restricts the importation to Hawai`i 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 tissue cultured plants in sterile media and containers are exempted from the ban. Other importations may be done by permit.

Meanwhile, in 2019, APHIS proposed to include all taxa in the Myrtaceae destined for Hawai`i in an existing regulatory category of “plants for planting” not authorized for importation pending pest risk assessment (NAPPRA). The intent was to reduce the probability of introduction of additional strains of Austropuccinia psidii to the Islands. This proposal appeared 14 years after the rust was first detected in Hawai`i. And the proposal has not yet taken effect. Therefore, imports of most living plants and cut foliage are still subject only to inspection (7 Code of Federal Regulations 319.37). The tiny size of the rust spores makes detection during inspection unlikely unless the plant is displaying symptoms of the disease.

Imports of logs and lumber involving tropical hardwood species (including Eucalyptus) into Hawai`i are regulated under separate provisions which have been in effect since 1995. The wood must be debarked or fumigated [Code of Federal Regulations – 7 CFR 319.40-5(c)]. Incoming wood packaging is regulated under ISPM#15; I think it unlikely that the treatments prescribed therein would kill any rust spores present.

Policy Responses in Other Vulnerable Countries

Australia

Austropuccinia psidii had been recognized as a potentially serious biosecurity threat to Australia as early as 1985 (publications cited by Carnegie et al. (2016). The introduction of ‘ōhi‘a rust to Hawai`i so alarmed plant health and conservation officials in Australia and New Zealand that they sent representatives half way around the world to participate in the North American Plant Protection Organization’s annual meeting in Newfoundland, Canada, in October 2007! Yet interest in Australia waned when large scale tree mortality and major impacts on industries did not immediately occur (Carnegie et al. 2016).  The state of New South Wales listed the rust as a Key Threatening Process to the Natural Environment, but the federal agencies rejected a petition to do the same at a national level (Carnegie et al. 2016).

Groups of scientists are carrying out research with the goal of demonstrating that the rust is already having severe effects on key species in natural ecosystems, and probably significantly affecting a wider range of species (Carnegie et al. 2016; Winzer et al. 2019; Winzer et al. 2020)

In 2018 a scientist affiliated with the Australian Network for Plant Conservation published a draft conservation plan.  Its 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

New Zealand has been more aggressive in its policy approach. It adopted a strategy when Australia announced arrival of the rust in 2010. The islands had bad luck – myrtle rust is believed to have been carried to New Zealand by wind from Australia across the Tasman Sea.

As soon as the rust was first detected in 2017, two government agencies initiated broad surveys of Myrtaceae across natural and urban areas, with active outreach to citizens (Toome-Heller et al. 2020).  By April 2018, it was recognized that the pathogen was too widespread to be eradicated. Significant finds were made on the western side of the North Island and at the very northern tip of the South Island (see map in Beresford et al. 2019). At that point, the government changed its focus to long-term management of the disease.

A. psidii is still very much a focus for Maori (indigenous) groups, central and local government, community groups, Myrtaceae-based industries, and research institutions.

Several research programmes are currently looking for management options, including resistance breeding (Toome-Heller et al. 2020). See research plan and reports of results to date here. However, which plant species can become infected, and under what environmental conditions, remain unclear.

New Zealand researchers have made some findings that should be of concern to forest pathologists working with all Myrtaceae:

• 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 and teliospores have only infrequently been found in New Zealand (Bereford et al. 2019).
• the unique biotype found in South Africa has already been found to be pathogenic towards some New Zealand native Myrtaceae  (Toome-Heller et al. 2020).

We can expect these finding to have implications for elsewhere, including in Hawaii.

Pathways of Introduction

It is thought probable that the rust was introduced to Hawai`i on cut foliage imported from Florida. The first Australian detection was at a cut flower facility (Australian Invasive Species Council).

CABI considers plants and plant parts (including cuttings, flowers, and germplasm) to be the principal pathway. Other pathways appear to be contaminated plant waste, timber, wood packaging and dunnage; and – over short distances – contaminated equipment and tools and clothing, shoes and other personal effects.

Conclusions

The saga of myrtle rust demonstrates both the biological and technical difficulties of controlling an airborne pathogen and the inability of the existing phytosanitary system to respond to new situations. Regulatory officials are obligated to demand levels of knowledge and certainty that just are not realistic. The gap is especially great at the crucial time – before an invasion or at its earliest stage — when phytosanitary actions might be most effective.

This saga also demonstrates that efforts often wane at the management and restoration stages. At least in Hawai`i and New Zealand, government resources are still being allocated to research possible resistance breeding or other possible long-term approaches. I refer you to the article by Enrico Bonello, me, and others about the need to provide sufficient resources to such efforts in the U.S.

Sources

Australian Invasive Species Council.2011. www.invasives.org.au Environmental impacts of myrtle rust Fact Sheet February 2011

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

Bonello, P. , F.T. Campbell, D. Cipollini, A.O. Conrad, C. Farinas, K.J.K. Gandhi, F.P. Hain, D. Parry, D.N. Showalter, C. Villari, and K.F. Wallin. 2019.  Invasive tree pests devastate ecosystems – A proposed new response framework. Frontiers  http://journal.frontiersin.org/article/10.3389/ffgc.2020.00002/full?&utm_source=Email_to_authors_&utm_medium=Email&utm_content=T1_11.5e1_author&utm_campaign=Email_publication&field=&journalName=Frontiers_in_Forests_and_Global_Change&id=510318

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).

Loope, L. and A.M. La Rosa. 2008. An Analysis of the Risk of Introduction of Additional Strains of the Rust Puccinia psidii Winter (`Ohi`a Rust) to Hawa`i.  Pacific Island Ecosystems Research Center

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

Toome-Heller, M. W.W.H. Ho, R.J. Ganley, C.E.A. Elliott, B. Quinn,  H.G. Pearson, B.J.R. Alexander. 2020. Chasing myrtle rust in New Zealand: host range and distribution over the first year after invasion. Australasian Plant Pathology

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)